Immune evasion by herpes simplex viruses;Evasión de la respuesta inmune por virus herpes simplex

Revista Chilena de Infectologia

Volumn 32, Issue 1, 2015, Pages 84-96

  Retamal Díaz, Angello R ^a,b   Suazo, Paula A ^a,b   Garrido, Ignacio ^a,b   Kalergis, Alexis M ^a,b   González, Pablo A ^a,b  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b Pontificia Universidad Católica de Chile   (Chile)

Author keywords

Adaptive immune evasion; Genital infection; Innate immune evasion; Latency; Reactivation

Indexed keywords

EID: 84926197961     PISSN: 07161018     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (169)

1. Looker K J, Garnett G P, Schmid G P. An estimate of the global prevalence and incidence of herpes simplex virus type 2 infection. Bull World Health Org 2008; 86: 805-12, A.
2. Schillinger J A, Xu F, Sternberg M R, Armstrong G L, Lee F K, Nahmias A J, et al. National seroprevalence and trends in herpes simplex virus type 1 in the United States, 1976-1994. Sex Transm Dis 2004; 31: 753-60.
3. Smith J S, Robinson N J. Age-specific prevalence of infection with herpes simplex virus types 2 and 1: a global review. J Infect Dis 2002; 186 Suppl 1: S3-28.
4. Chayavichitsilp P, Buckwalter J V, Krakowski A C, Friedlander S F. Herpes simplex. Pediatr Rev 2009; 30: 119-29; quiz 30.
5. Farooq A V, Shukla D. Herpes simplex epithelial and stromal keratitis: an epidemiologic update. Surv Ophthalmol 2012; 57: 448-62.
6. Kaye S, Choudhary A. Herpes simplex keratitis. Prog Retin Eye Res 2006; 25: 355-80.
7. Lafferty W E, Coombs R W, Benedetti J, Critchlow C, Corey L. Recurrences after oral and genital herpes simplex virus infection. Influence of site of infection and viral type. N Engl J Med 1987; 316: 1444-9.
8. Mertz K J, Trees D, Levine W C, Lewis J S, Litchfield B, Pettus K S, et al. Etiology of genital ulcers and prevalence of human immunodeficiency virus coinfection in 10 US cities. The Genital Ulcer Disease Surveillance Group. J Infect Dis 1998; 178: 1795-8.
9. Paz-Bailey G, Rahman M, Chen C, Ballard R, Moffat H J, Kenyon T, et al. Changes in the etiology of sexually transmitted diseases in Botswana between 1993 and 2002: implications for the clinical management of genital ulcer disease. Clin Infect Dis 2005; 41: 1304-12.
10. Kimberlin D. Herpes simplex virus, meningitis and encephalitis in neonates. Herpes 2004; 11 Suppl 2: 65A-76A.
11. Ward K N, Ohrling A, Bryant N J, Bowley J S, Ross E M, Verity C M. Herpes simplex serious neurological disease in young children: incidence and long-term outcome. Arch Dis Child 2012; 97: 162-5.
12. Freeman E E, Weiss H A, Glynn J R, Cross P L, Whitworth J A, Hayes R J. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and metaanalysis of longitudinal studies. AIDS 2006; 20: 73-83.
13. Gray R H, Wawer M J, Brookmeyer R, Sewankambo N K, Serwadda D, Wabwire-Mangen F, et al. Probability of HIV-1 transmission per coital act in monogamous, heterosexual, HIV-1-discordant couples in Rakai, Uganda. Lancet 2001; 357: 1149-53.
14. Wald A, Link K. Risk of human immunodeficiency virus infection in herpes simplex virus type 2-seropositive persons: a meta-analysis. J Infect Dis 2002; 185: 45-52.
15. Paz-Bailey G, Ramaswamy M, Hawkes S J, Geretti A M. Herpes simplex virus type 2: epidemiology and management options in developing countries. Sex Transm Infect 2007; 83: 16-22.
16. Doi Y, Ninomiya T, Hata J, Yonemoto K, Tanizaki Y, Arima H, et al. Seroprevalence of herpes simplex virus 1 and 2 in a populationbased cohort in Japan. J Epidemiol 2009; 19: 56-62.
17. Bernstein D I, Bellamy A R, Hook E W 3rd, Levin M J, Wald A, Ewell M G, et al. Epidemiology, clinical presentation, and antibody response to primary infection with herpes simplex virus type 1 and type 2 in young women. Clin Infect Dis 2013; 56: 344-51.
18. Suárez M, Briones H, Dubinovsky S, Aliaga P, Alarcón G, Diego S D, et al. Infección genital herpética en estudiantes universitarias chilenas. Bol. Oficina Sanit. Panam 1989; 106: 389-95.
19. Wald A, Corey L, Cone R, Hobson A, Davis G, Zeh J. Frequent genital herpes simplex virus 2 shedding in immunocompetent women. Effect of acyclovir treatment. J Clin Invest 1997; 99: 1092-7.
20. Martínez M J, Navarrete N, Santander E, Garmendia M L, Gubelin W. Seropervalencia de la infección por virus herpes simplex tipo 2 en pacientes atendidos en centros de referencia de ETS de Santiago. Rev Med Chile 2005; 133: 302-6.
21. Carcamo C P, Campos P E, García P J, Hughes J P, Garnett G P, Holmes K K, et al. Prevalences of sexually transmitted infections in young adults and female sex workers in Peru: a national population-based survey. Lancet Infect Dis 2012; 12: 765-73.
22. Clemens S A, Farhat C K. Seroprevalence of herpes simplex 1-2 antibodies in Brazil. Rev Saude Publica 2010; 44: 726-34.
23. Cowan F M, French R S, Mayaud P, Gopal R, Robinson N J, de Oliveira S A, et al. Seroepidemiological study of herpes simplex virus types 1 and 2 in Brazil, Estonia, India, Morocco, and Sri Lanka. Sex Transm Infect 2003; 79: 286-90.
24. Schiffer J T, Corey L. Rapid host immune response and viral dynamics in herpes simplex virus-2 infection. Nat Med 2013; 19: 280-90.
25. Dolan A, Jamieson F E, Cunningham C, Barnett B C, McGeoch D J. The genome sequence of herpes simplex virus type 2. J Virol 1998; 72: 2010-21.
26. Dohner K, Wolfstein A, Prank U, Echeverri C, Dujardin D, Vallee R, et al. Function of dynein and dynactin in herpes simplex virus capsid transport. Mol Biol Cell 2002; 13: 2795-809.
27. Granzow H, Klupp B G, Mettenleiter T C. Entry of pseudorabies virus: an immunogold-labeling study. J Virol 2005; 79: 3200-5.
28. Rajcani J, Vojvodova A. The role of herpes simplex virus glycoproteins in the virus replication cycle. Acta Virol 1998; 42: 103-18.
29. Akhtar J, Shukla D. Viral entry mechanisms: cellular and viral mediators of herpes simplex virus entry. FEBS J 2009; 276: 7228-36.
30. Avitabile E, Forghieri C, Campadelli-Fiume G. Cross talk among the glycoproteins involved in herpes simplex virus entry and fusion: the interaction between gB and gH/gL does not necessarily require gD. J Virol 2009; 83: 10752-60.
31. Turner A, Bruun B, Minson T, Browne H. Glycoproteins gB, gD, and gHgL of herpes simplex virus type 1 are necessary and sufficient to mediate membrane fusion in a Cos cell transfection system. J Virol 1998; 72: 873-5.
32. Atanasiu D, Cairns T M, Whitbeck J C, Saw W T, Rao S, Eisenberg R J, et al. Regulation of herpes simplex virus gB-induced cell-cell fusion by mutant forms of gH/gL in the absence of gD and cellular receptors. MBio 2013; 4 (2). pii: e00046-13. doi: 10.1128?mBio.00046-13.
33. Herold B C, WuDunn D, Soltys N, Spear P G. Glycoprotein C of herpes simplex virus type 1 plays a principal role in the adsorption of virus to cells and in infectivity. J Virol 1991; 65: 1090-8.
34. Krummenacher C, Baribaud F, Ponce de León M, Baribaud I, Whitbeck JC, Xu R, et al. Comparative usage of herpesvirus entry mediator A and nectin-1 by laboratory strains and clinical isolates of herpes simplex virus. Virology 2004; 322: 286-99.
35. Lazear E, Whitbeck J C, Zuo Y, Carfí A, Cohen G H, Eisenberg R J, et al. Induction of conformational changes at the N-terminus of herpes simplex virus glycoprotein D upon binding to HVEM and nectin-1. Virology 2014; 448: 185-95.
36. Matsushima H, Utani A, Endo H, Matsuura H, Kakuta M, Nakamura Y, et al. The expression of nectin-1α in normal human skin and various skin tumours. Br J Dermatol 2003; 148: 755-62.
37. Steinberg M W, Huang Y, Wang-Zhu Y, Ware C F, Cheroutre H, Kronenberg M. BTLA interaction with HVEM expressed on CD8+ T cells promotes survival and memory generation in response to a bacterial infection. PLoS One 2013; 8: e77992.
38. Fusco D, Forghieri C, Campadelli-Fiume G. The pro-fusion domain of herpes simplex virus glycoprotein D (gD) interacts with the gD N terminus and is displaced by soluble forms of viral receptors. Proc Natl Acad Sci U S A 2005; 102: 9323-8.
39. Krummenacher C, Supekar V M, Whitbeck J C, Lazear E, Connolly S A, Eisenberg R J, et al. Structure of unliganded HSV gD reveals a mechanism for receptor-mediated activation of virus entry. EMBO J 2005; 24: 4144-53.
40. Silva L, Oh H S, Chang L, Yan Z, Triezenberg S J, Knipe D M. Roles of the nuclear lamina in stable nuclear association and assembly of a herpesviral transactivator complex on viral immediate-early genes. MBio 2012; 3 (1). pii: e00300-11. doi: 10.1128?mBio.00300-1.
41. Wu W, Guo Z, Zhang X, Guo L, Liu L, Liao Y, et al. A microRNA encoded by HSV-1 inhibits a cellular transcriptional repressor of viral immediate early and early genes. Sci China Life Sci 2013; 56: 373-83.
42. Jackson S A, DeLuca N A. Relationship of herpes simplex virus genome configuration to productive and persistent infections. Proc Natl Acad Sci U S A 2003; 100: 7871-6.
43. Chen S, Mills L, Perry P, Riddle S, Wobig R, Lown R, et al. Transactivation of the major capsid protein gene of herpes simplex virus type 1 requires a cellular transcription factor. J Virol 1992; 66: 4304-14.
44. Rajcani J, Andrea V, Ingeborg R. Peculiarities of herpes simplex virus (HSV) transcription: an overview. Virus Genes 2004; 28: 293-310.
45. Granzow H, Klupp B G, Fuchs W, Veits J, Osterrieder N, Mettenleiter T C. Egress of alphaherpesviruses: comparative ultrastructural study. J Virol 2001; 75: 3675-84.
46. Johnson D C, Baines J D. Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 2011; 9: 382-94.
47. Nii S, Morgan C, Rose H M. Electron microscopy of herpes simplex virus. II. Sequence of development. J Virol 1968; 2: 517-36.
48. Darlington R W, Moss L H, 3rd. Herpesvirus envelopment. J Virol 1968; 2: 48-55.
49. Turcotte S, Letellier J, Lippe R. Herpes simplex virus type 1 capsids transit by the trans-Golgi network, where viral glycoproteins accumulate independently of capsid egress. J Virol 2005; 79: 8847-60.
50. Johnson D C, Webb M, Wisner T W, Brunetti C. Herpes simplex virus gE/gI sorts nascent virions to epithelial cell junctions, promoting virus spread. J Virol 2001; 75: 821-33.
51. Aubert M, Yoon M, Sloan D D, Spear P G, Jerome K R. The virological synapse facilitates herpes simplex virus entry into T cells. J Virol 2009; 83: 6171-83.
52. Lubinski J M, Lazear H M, Awasthi S, Wang F, Friedman H M. The herpes simplex virus 1 IgG Fc receptor blocks antibodymediated complement activation and antibodydependent cellular cytotoxicity in vivo. J Virol 2011; 85: 3239-49.
53. Hook L M, Lubinski J M, Jiang M, Pangburn M K, Friedman H M. Herpes simplex virus type 1 and 2 glycoprotein C prevents complement-mediated neutralization induced by natural immunoglobulin M antibody. J Virol 2006; 80: 4038-46.
54. Corey L, Spear P G. Infections with herpes simplex viruses 1. N Engl J Med 1986; 314: 686-91.
55. Obara Y, Furuta Y, Takasu T, Suzuki S, Suzuki H, Matsukawa S, et al. Distribution of herpes simplex virus types 1 and 2 genomes in human spinal ganglia studied by PCR and in situ hybridization. J Med Virol 1997; 52: 136-42.
56. Pevenstein S R, Williams R K, McChesney D, Mont E K, Smialek J E, Straus S E. Quantitation of latent varicella-zoster virus and herpes simplex virus genomes in human trigeminal ganglia. J Virol 1999; 73: 10514-8.
57. Stevens J G, Cook M L. Latent herpes simplex virus in spinal ganglia of mice. Science 1971; 173: 843-5.
58. Antinone S E, Smith G A. Retrograde axon transport of herpes simplex virus and pseudorabies virus: a live-cell comparative analysis. J Virol 2010; 84: 1504-12.
59. Mellerick D M, Fraser N W. Physical state of the latent herpes simplex virus genome in a mouse model system: evidence suggesting an episomal state. Virology 1987; 158: 265-75.
60. Goins W F, Wolfe D, Krisky D M, Bai Q, Burton E A, Fink D J, et al. Delivery using herpes simplex virus: an overview. Methods Mol Biol 2004; 246: 257-99.
61. Stevens J G, Wagner E K, Devi-Rao G B, Cook M L, Feldman L T. RNA complementary to a herpesvirus alpha gene mRNA is prominent in latently infected neurons. Science 1987; 235: 1056-9.
62. Umbach J L, Kramer M F, Jurak I, Karnowski H W, Coen D M, Cullen B R. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008; 454: 780-3.
63. Kenny J J, Krebs F C, Hartle H T, Gartner A E, Chatton B, Leiden J M, et al. Identification of a second ATF/CREB-like element in the herpes simplex virus type 1 (HSV-1) latency-associated transcript (LAT) promoter. Virology 1994; 200: 220-35.
64. Oh J, Fraser N W. Temporal association of the herpes simplex virus genome with histone proteins during a lytic infection. J Virol 2008; 82: 3530-7.
65. Huang J, Kent J R, Placek B, Whelan K A, Hollow C M, Zeng P Y, et al. Trimethylation of histone H3 lysine 4 by Set1 in the lytic infection of human herpes simplex virus 1. J Virol 2006; 80: 5740-6.
66. Cliffe A R, Knipe D M. Herpes simplex virus ICP0 promotes both histone removal and acetylation on viral DNA during lytic infection. J Virol 2008; 82: 12030-8.
67. Hobbs W E, 2nd, DeLuca N A. Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J Virol 1999; 73: 8245-55.
68. Du T, Zhou G, Roizman B. Induction of apoptosis accelerates reactivation of latent HSV-1 in ganglionic organ cultures and replication in cell cultures. Proc Natl Acad Sci U S A 2012; 109: 14616-21.
69. Kobayashi M, Wilson A C, Chao M V, Mohr I. Control of viral latency in neurons by axonal mTOR signaling and the 4E-BP translation repressor. Genes Dev 2012; 26: 1527-32.
70. Spruance S L. Cutaneous herpes simplex virus lesions induced by ultraviolet radiation. A review of model systems and prophylactic therapy with oral acyclovir. Am J Med 1988; 85: 43-5.
71. Huang W, Xie P, Xu M, Li P, Zao G. The influence of stress factors on the reactivation of latent herpes simplex virus type 1 in infected mice. Cell Biochem Biophys 2011; 61: 115-22.
72. Lautenschlager S, Eichmann A. The heterogeneous clinical spectrum of genital herpes. Dermatology 2001; 202: 211-9.
73. Wald A, Zeh J, Selke S, Warren T, Ryncarz A J, Ashley R, et al. Reactivation of genital herpes simplex virus type 2 infection in asymptomatic seropositive persons. N Engl J Med 2000; 342: 844-50.
74. Mertz G J, Benedetti J, Ashley R, Selke S A, Corey L. Risk factors for the sexual transmission of genital herpes. Ann Intern Med 1992; 116: 197-202.
75. Fleming D T, McQuillan G M, Johnson R E, Nahmias A J, Aral S O, Lee F K, et al. Herpes simplex virus type 2 in the United States, 1976 to 1994. N Engl J Med 1997; 337: 1105-11.
76. Cowan F M, Johnson A M, Ashley R, Corey L, Mindel A. Antibody to herpes simplex virus type 2 as serological marker of sexual lifestyle in populations. BMJ 1994; 309: 1325-9.
77. Solomon L, Cannon M J, Reyes M, Graber J M, Wetherall N T, Reeves W C, et al. Epidemiology of recurrent genital herpes simplex virus types 1 and 2. Sex Transm Infect 2003; 79: 456-9.
78. Janier M, Scieux C, Meouchi R, Tournoux C, Porcher R, Maillard A, et al. Virological, serological and epidemiological study of 255 consecutive cases of genital herpes in a sexually transmitted disease clinic of Paris (France): a prospective study. Int J STD AIDS 2006; 17: 44-9.
79. Benedetti J, Corey L, Ashley R. Recurrence rates in genital herpes after symptomatic firstepisode infection. Ann Intern Med 1994; 121: 847-54.
80. Margolis T P, Imai Y, Yang L, Vallas V, Krause P R. Herpes simplex virus type 2 (HSV-2) establishes latent infection in a different population of ganglionic neurons than HSV-1: role of latency-associated transcripts. J Virol 2007; 81: 1872-8.
81. Ashkar A A, Yao X D, Gill N, Sajic D, Patrick A J, Rosenthal KL. Toll-like receptor (TLR)-3, but not TLR4, agonist protects against genital herpes infection in the absence of inflammation seen with CpG DNA. J Infect Dis 2004; 190: 1841-9.
82. Miller R L, Imbertson L M, Reiter M J, Gerster J F. Treatment of primary herpes simplex virus infection in guinea pigs by imiquimod. Antiviral Res 1999; 44: 31-42.
83. Harandi A M, Eriksson K, Holmgren J. A protective role of locally administered immunostimulatory CpG oligodeoxynucleotide in a mouse model of genital herpes infection. J Virol 2003; 77: 953-62.
84. Pyles R B, Higgins D, Chalk C, Zalar A, Eiden J, Brown C, et al. Use of immunostimulatory sequence-containing oligonucleotides as topical therapy for genital herpes simplex virus type 2 infection. J Virol 2002; 76: 11387-96.
85. Theofilopoulos A N, Baccala R, Beutler B, Kono D H. Type I interferons (alpha/beta) in immunity and autoimmunity. Annu Rev Immunol 2005; 23: 307-36.
86. Al-khatib K, Williams B R G, Robert H, Halford W, Carr D J J. Distinctive roles for 2’,5’-oligoadenylate synthetases and doublestranded RNA-dependent protein kinase R in the in vivo antiviral effect of an adenoviral vector expressing murine IFN-β. JImmunol 2004; 172: 5638-47.
87. Alexopoulou L, Holt A C, Medzhitov R, Flavell R A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001; 413: 732-8.
88. Diebold S S, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of singlestranded RNA. Science 2004; 303: 1529-31.
89. Hemmi H, Kaisho T, Takeuchi O, Sato S, Sanjo H, Hoshino K, et al. Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat Immunol 2002; 3: 196-200.
90. Shu M, Taddeo B, Zhang W, Roizman B. Selective degradation of mRNAs by the HSV host shutoff RNase is regulated by the UL47 tegument protein. Proc Natl Acad Sci U S A 2013; 110: E1669-75.
91. Everly D N Jr, Read G S. Mutational analysis of the virion host shutoff gene (UL41) of herpes simplex virus (HSV): characterization of HSV type 1 (HSV-1)/HSV-2 chimeras. J Virol 1997; 71: 7157-66.
92. Yao X D, Rosenthal K L. Herpes simplex virus type 2 virion host shutoff protein suppresses innate dsRNA antiviral pathways in human vaginal epithelial cells. J Gen Virol 2011; 92: 1981-93.
93. Peng T, Zhu J, Klock A, Phasouk K, Huang M L, Koelle D M, et al. Evasion of the mucosal innate immune system by herpes simplex virus type 2. J Virol 2009; 83: 12559-68.
94. Johnson K E, Song B, Knipe D M. Role for herpes simplex virus 1 ICP27 in the inhibition of type I interferon signaling. Virology 2008; 374: 487-94.
95. Shupack J, Stiller M, Davis I, Kenny C, Jondreau L. Topical alpha-interferon ointment with dimethyl sulfoxide in the treatment of recurrent genital herpes simplex. Dermatology 1992; 184: 40-4.
96. Hirokawa D, Woldow A, Lee S N, Samie F. Treatment of recalcitrant herpes simplex virus with topical imiquimod. Cutis 2011; 88: 276-7.
97. Kan Y, Okabayashi T, Yokota S, Yamamoto S, Fujii N, Yamashita T. Imiquimod suppresses propagation of herpes simplex virus 1 by upregulation of cystatin A via the adenosine receptor A1 pathway. J Virol 2012; 86: 10338-46.
98. Lascaux A S, Caumes E, Deback C, Melica G, Challine D, Agut H, et al. Successful treatment of aciclovir and foscarnet resistant Herpes simplex virus lesions with topical imiquimod in patients infected with human immunodeficiency virus type 1. J Med Virol 2012; 84: 194-7.
99. Carr D J J, Tomanek L, Silverman R H, Iain L, Williams B R G, Campbell IL. RNA-dependent protein kinase is required for alpha-1 interferon transgene-induced resistance to genital herpes simplex virus type 2. J Virol 2005; 79: 9341-5.
100. Leib D A, Machalek M A, Williams B R, Silverman R H, Virgin H W. Specific phenotypic restoration of an attenuated virus by knockout of a host resistance gene. Proc Natl Acad Sci USA 2000; 97: 6097--101.
101. He B, Gross M, Roizman B. The γ34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1α to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNAactivated protein kinase. Proc Natl Acad Sci U S A 1997; 94: 843-8.
102. Poppers J, Mulvey M, Khoo D, Mohr I. Inhibition of PKR activation by the proline-rich RNA binding domain of the herpes simplex virus type 1 Us11 protein. J Virol 2000; 74: 11215-21.
103. Fakioglu E, Wilson S S, Mesquita P M, Hazrati E, Cheshenko N, Blaho J A, et al. Herpes simplex virus downregulates secretory leukocyte protease inhibitor: a novel immune evasion mechanism. J Virol 2008; 82: 9337-44.
104. Nguyen M L, Blaho J A. Apoptosis during herpes simplex virus infection. Adv Virus Res 2007; 69: 67-97.
105. Morton E R, Blaho J A. Herpes simplex virus blocks Fas-mediated apoptosis independent of viral activation of NF-kappaB in human epithelial HEp-2 cells. J Interferon Cytokine Res 2007; 27: 365-76.
106. Aubert M, Krantz E M, Jerome K R. Herpes simplex virus genes Us3, Us5, and Us12 differentially regulate cytotoxic T lymphocyteinduced cytotoxicity. Viral Immunol 2006; 19: 391-408.
107. Zhou G, Galvan V, Campadelli-Fiume G, Roizman B. Glycoprotein D or J delivered in trans blocks apoptosis in SK-N-SH cells induced by a herpes simplex virus 1 mutant lacking intact genes expressing both glycoproteins. J Virol 2000; 74: 11782-91.
108. Yamauchi Y, Daikoku T, Goshima F, Nishiyama Y. Herpes simplex virus UL14 protein blocks apoptosis. Microbiol Immunol 2003; 47: 685-9.
109. Golembewski E K, Wales S Q, Aurelian L, Yarowsky P J. The HSV-2 protein ICP10PK prevents neuronal apoptosis and loss of function in an in vivo model of neurodegeneration associated with glutamate excitotoxicity. Exp Neurol 2007; 203: 381-93.
110. Lubinski J M, Jiang M, Hook L, Chang Y, Sarver C, Mastellos D, et al. Herpes simplex virus type 1 evades the effects of antibody and complement in vivo. J Virol 2002; 76: 9232-41.
111. Godfrey D I, Pellicci D G, Patel O, Kjer-Nielsen L, McCluskey J, Rossjohn J. Antigen recognition by CD1d-restricted NKT T cell receptors. Semin Immunol 2010; 22: 61-7.
112. Rao P, Pham HT, Kulkarni A, Yang Y, Liu X, Knipe D M, et al. Herpes simplex virus 1 glycoprotein B and US3 collaborate to inhibit CD1d antigen presentation and NKT cell function. J Virol 2011; 85: 8093-104.
113. Yuan W, Dasgupta A, Cresswell P. Herpes simplex virus evades natural killer T cell recognition by suppressing CD1d recycling. Nat Immunol 2006; 7: 835-42.
114. Puttur F K, Fernández M A, White R, Roediger B, Cunningham A L, Weninger W, et al. Herpes simplex virus infects skin γδT cells before Langerhans cells and impedes migration of infected Langerhans cells by inducing apoptosis and blocking E-cadherin downregulation. J Immunol 2010; 185: 477-87.
115. Kim J O, Cha H R, Kim E D, Kweon M N. Pathological effect of IL-17A-producing TCRgammadelta(+) T cells in mouse genital mucosa against HSV-2 infection. Immunol Lett 2012; 147: 34-40.
116. Iannello A, Debbeche O, El Arabi R, Samarani S, Hamel D, Rozenberg F, et al. Herpes simplex virus type 1-induced FasL expression in human monocytic cells and its implications for cell death, viral replication, and immune evasion. Viral Immunol 2011; 24: 11-26.
117. Schepis D, D’Amato M, Studahl M, Bergstrom T, Karre K, Berg L. Herpes simplex virus infection downmodulates NKG2D ligand expression. Scand J Immunol 2009; 69: 429-36.
118. Tomazin R, Hill A, Jugovic P, York I, Van Endert P, Ploegh H, et al. Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP. EMBO J 1996; 15: 3256.
119. Halford W P, Maender J L, Gebhardt B M. Re-evaluating the role of natural killer cells in innate resistance to herpes simplex virus type 1. Virol J 2005; 2: 56.
120. Nandakumar S, Woolard S N, Yuan D, Rouse B T, Kumaraguru U. Natural killer cells as novel helpers in anti-herpes simplex virus immune response. J Virol 2008; 82: 10820-31.
121. Para M F, Goldstein L, Spear P G. Similarities and differences in the Fc-binding glycoprotein (gE) of herpes simplex virus types 1 and 2 and tentative mapping of the viral gene for this glycoprotein. J Virol 1982; 41: 137-44.
122. Armour K L, Atherton A, Williamson L M, Clark M R. The contrasting IgG-binding interactions of human and herpes simplex virus Fc receptors. Biochem Soc Trans 2002; 30: 495-500.
123. Dilillo D J, Tan G S, Palese P, Ravetch J V. Broadly neutralizing hemagglutinin stalkspecific antibodies require FcγR interactions for protection against influenza virus in vivo. Nat Med 2014; 20: 143-51.
124. Carreno L J, González P A, Bueno S M, Riedel C A, Kalergis A M. Modulation of the dendritic cell-T-cell synapse to promote pathogen immunity and prevent autoimmunity. Immunotherapy 2011; 3: 6-11.
125. González P A, Prado C E, Leiva E D, Carreno L J, Bueno S M, Riedel C A, et al. Respiratory syncytial virus impairs T cell activation by preventing synapse assembly with dendritic cells. Proc Natl Acad Sci U S A 2008; 105: 14999-5004.
126. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000; 18: 767-811.
127. González P A, Carreno L J, Figueroa C A, Kalergis A M. Modulation of immunological synapse by membrane-bound and soluble ligands. Cytokine Growth Factor Rev 2007; 18: 19-31.
128. Tobar J A, González P A, Kalergis A M. Salmonella escape from antigen presentation can be overcome by targeting bacteria to Fc gamma receptors on dendritic cells. J Immunol 2004; 173: 4058-65.
129. Tobar J A, Carreno L J, Bueno S M, González P A, Mora J E, Quezada S A, et al. Virulent Salmonella enterica serovar typhimurium evades adaptive immunity by preventing dendritic cells from activating T cells. Infect Immun 2006; 74: 6438-48.
130. Raftery M J, Winau F, Kaufmann S H, Schaible U E, Schonrich G. CD1 antigen presentation by human dendritic cells as a target for herpes simplex virus immune evasion. J Immunol 2006; 177: 6207-14.
131. Majumder B, Janket M L, Schafer E A, Schaubert K, Huang X L, Kan-Mitchell J, et al. Human immunodeficiency virus type 1 Vpr impairs dendritic cell maturation and T-cell activation: implications for viral immune escape. J Virol 2005; 79: 7990-8003.
132. Morrow G, Slobedman B, Cunningham AL, Abendroth A. Varicella-zoster virus productively infects mature dendritic cells and alters their immune function. J Virol 2003; 77: 4950-9.
133. Bueno S M, González P A, Carreno L J, Tobar J A, Mora G C, Pereda C J, et al. The capacity of Salmonella to survive inside dendritic cells and prevent antigen presentation to T cells is host specific. Immunology 2008; 124: 522-33.
134. Bosnjak L, Miranda-Saksena M, Koelle D M, Boadle R A, Jones C A, Cunningham AL. Herpes simplex virus infection of human dendritic cells induces apoptosis and allows cross-presentation via uninfected dendritic cells. J Immunol 2005; 174: 2220-7.
135. Stefanidou M, Ramos I, Mas Casullo V, Trepanier J B, Rosenbaum S, Fernández-Sesma A, et al. Herpes simplex virus 2 (HSV-2) prevents dendritic cell maturation, induces apoptosis, and triggers release of proinflammatory cytokines: potential links to HSV-HIV synergy. J Virol 2013; 87: 1443-53.
136. Gobeil P A, Leib D A. Herpes simplex virus γ34.5 interferes with autophagosome maturation and antigen presentation in dendritic cells. MBio 2012; 3: e00267-12.
137. Yordy B, Iijima N, Huttner A, Leib D, Iwasaki A. A neuron-specific role for autophagy in antiviral defense against herpes simplex virus. Cell Host Microbe 2012; 12: 334-45.
138. Hill A B, Barnett B C, McMichael A J, McGeoch D J. HLA class I molecules are not transported to the cell surface in cells infected with herpes simplex virus types 1 and 2. JImmunol 1994; 152: 2736-41.
139. Hill A, Jugovic P, York I, Russ G, Bennink J, Yewdell J, et al. Herpes simplex virus turns off the TAP to evade host immunity. Nature 1995; 375: 411-5.
140. Imai T, Koyanagi N, Ogawa R, Shindo K, Suenaga T, Sato A, et al. Us3 kinase encoded by herpes simplex virus 1 mediates downregulation of cell surface major histocompatibility complex class I and evasion of CD8+ T cells. PLoS One 2013; 8: e72050.
141. Elboim M, Grodzovski I, Djian E, Wolf D G, Mandelboim O. HSV-2 specifically down regulates HLA-C expression to render HSV-2-infected DCs susceptible to NK cell killing. PLoS Pathog 2013; 9: e1003226.
142. Jerome K R, Fox R, Chen Z, Sears A E, Lee H, Corey L. Herpes simplex virus inhibits apoptosis through the action of two genes, Us5 and Us3. J Virol 1999; 73: 8950-7.
143. Vanden Oever M J, Han J Y. Caspase 9 is essential for herpes simplex virus type 2-induced apoptosis in T cells. J Virol 2010; 84: 3116-20.
144. Jerome K R, Chen Z, Lang R, Torres M R, Hofmeister J, Smith S, et al. HSV and glycoprotein J inhibit caspase activation and apoptosis induced by granzyme B or Fas. J Immunol 2001; 167: 3928-35.
145. Raftery M J, Behrens C K, Muller A, Krammer P H, Walczak H, Schonrich G. Herpes simplex virus type 1 infection of activated cytotoxic T cells: Induction of fratricide as a mechanism of viral immune evasion. J Exp Med 1999; 190: 1103-14.
146. La S, Kim J, Kwon B S, Kwon B. Herpes simplex virus type 1 glycoprotein D inhibits T-cell proliferation. Mol Cells 2002; 14: 398-403.
147. Sloan D D, Han J Y, Sandifer T K, Stewart M, Hinz A J, Yoon M, et al. Inhibition of TCR signaling by herpes simplex virus. J Immunol 2006; 176: 1825-33.
148. Cheung T C. Modulation of T cell proliferation through the LIGHT-HVEM-BTLA cosignaling pathway. Recent Pat DNA Gene Seq 2009; 3: 177-82.
149. Fernández M A, Puttur F K, Wang Y M, Howden W, Alexander S I, Jones C A. T regulatory cells contribute to the attenuated primary CD8+ and CD4+ T cell responses to herpes simplex virus type 2 in neonatal mice. J Immunol 2008; 180: 1556-64.
150. Suvas S, Kumaraguru U, Pack CD, Lee S, Rouse B T. CD4+CD25+ T cells regulate virusspecific primary and memory CD8+ T cell responses. J Exp Med 2003; 198: 889-901.
151. Fernández M A, Yu U, Zhang G, White R, Sparwasser T, Alexander S I, et al. Treg depletion attenuates the severity of skin disease from ganglionic spread after HSV-2 flank infection. Virology 2013; 447: 9-20.
152. Iyer A V, Pahar B, Chouljenko V N, Walker J D, Stanfield B, Kousoulas K G. Single dose of Glycoprotein K (gK)-deleted HSV-1 liveattenuated virus protects mice against lethal vaginal challenge with HSV-1 and HSV-2 and induces lasting T cell memory immune responses. Virol J 2013; 10: 317.
153. Lund J M, Hsing L, Pham T T, Rudensky A Y. Coordination of early protective immunity to viral infection by regulatory T cells. Science 2008; 320: 1220-4.
154. Burchett S K, Corey L, Mohan K M, Westall J, Ashley R, Wilson CB. Diminished interferongamma and lymphocyte proliferation in neonatal and postpartum primary herpes simplex virus infection. J Infect Dis 1992; 165: 813-8.
155. Evans I A, Jones C A. HSV induces an early primary Th1 CD4 T cell response in neonatal mice, but reduced CTL activity at the time of the peak adult response. Eur J Immunol 2005; 35: 1454-62.
156. Awasthi S, Friedman H M. Status of prophylactic and therapeutic genital herpes vaccines. Curr Opin Virol 2014; 6C: 6-12.
157. Bernstein D I, Aoki F Y, Tyring S K, Stanberry L R, St-Pierre C, Shafran S D, et al. Safety and immunogenicity of glycoprotein D-adjuvant genital herpes vaccine. Clin Infect Dis 2005; 40: 1271-81.
158. Johnston C, Koelle D M, Wald A. Current status and prospects for development of an HSV vaccine. Vaccine 2014; 32: 1553-60.
159. Belshe R B, Leone P A, Bernstein D I, Wald A, Levin M J, Stapleton J T, et al. Efficacy results of a trial of a herpes simplex vaccine. N Engl J Med 2012; 366: 34-43.
160. Gershon A A. Varicella zoster vaccines and their implications for development of HSV vaccines. Virology 2013; 435: 29-36.
161. Goldman G S, King P G. Review of the United States universal varicella vaccination program: Herpes zoster incidence rates, cost-effectiveness, and vaccine efficacy based primarily on the antelope valley varicella active surveillance project data. Vaccine 2013; 31: 1680-94.
162. de Bruyn G, Vargas-Cortez M, Warren T, Tyring S K, Fife K H, Lalezari J, et al. A randomized controlled trial of a replication defective (gH deletion) herpes simplex virus vaccine for the treatment of recurrent genital herpes among immunocompetent subjects. Vaccine 2006; 24: 914-20.
163. Casanova G, Cancela R, Alonzo L, Benuto R. A double-blind study of the efficacy and safety of the ICP10PK vaccine against recurrent genital HSV-2 infections. Cutis 2002.
164. Halford W P, Puschel R, Gershburg E, Wilber A, Gershburg S, Rakowski B. A liveattenuated HSV-2 ICP0 virus elicits 10 to 100 times greater protection against genital herpes than a glycoprotein D subunit vaccine. PLoS One 2011; 6: e17748.
165. Da Costa X, Kramer M F, Zhu J, Brockman M A, Knipe D M. Construction, phenotypic analysis, and immunogenicity of a UL5/UL29 double deletion mutant of herpes simplex virus 2. J Virol 2000; 74: 7963-71.
166. Mundle S T, Hernández H, Hamberger J, Catalan J, Zhou C, Stegalkina S, et al. Highpurity preparation of HSV-2 vaccine candidate ACAM529 is immunogenic and efficacious in vivo. PLoS One 2013; 8: e57224.
167. Awasthi S, Zumbrun E E, Si H, Wang F, Shaw C E, Cai M, et al. Live attenuated herpes simplex virus 2 glycoprotein E deletion mutant as a vaccine candidate defective in neuronal spread. J Virol 2012; 86: 4586-98.
168. Kolb A W, Ane C, Brandt C R. Using HSV-1 Genome phylogenetics to track past human migrations. PLoS One 2013; 8: e76267.
169. Awasthi S, Lubinski J M, Shaw C E, Barrett S M, Cai M, Wang F, et al. Immunization with a vaccine combining herpes simplex virus 2 (HSV-2) glycoprotein C (gC) and gD subunits improves the protection of dorsal root ganglia in mice and reduces the frequency of recurrent vaginal shedding of HSV-2 DNA in guinea pigs compared to immunization with gD alone. J Virol 2011; 85: 10472-86.