Varicella Viruses Inhibit Interferon-Stimulated JAK-STAT Signaling through Multiple Mechanisms

PLoS Pathogens

Volumn 11, Issue 5, 2015, Pages

  Verweij, Marieke C ^a   Wellish, Mary ^b   Whitmer, Travis ^a   Malouli, Daniel ^a   Lapel, Martin ^b   Jonjić, Stipan ^c   Haas, Juergen G ^d   DeFilippis, Victor R ^a   Mahalingam, Ravi ^b   Früh, Klaus ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF RIJEKA   (Croatia)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; JANUS KINASE; STAT PROTEIN; IMMEDIATE EARLY PROTEIN; INTERFERON REGULATORY FACTOR 9; PROTEASOME; RECOMBINANT DNA; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VARICELLA ZOSTER VIRUS; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CERCOPITHECINAE; CHICKENPOX; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; HERPES VIRUS INFECTION; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INNATE IMMUNITY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN PROCESSING; VARICELLOVIRUS; VIROLOGY;

ANIMALIA; CERCOPITHECINE HERPESVIRUS 9; HUMAN HERPESVIRUS 3; MACACA MULATTA; SAL VIEJA VIRUS;

ANIMALS; CELL LINE; CERCOPITHECINAE; CHICKENPOX; DNA, RECOMBINANT; GENE EXPRESSION REGULATION, VIRAL; HERPESVIRIDAE INFECTIONS; HERPESVIRUS 3, HUMAN; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMEDIATE-EARLY PROTEINS; IMMUNITY, INNATE; INTERFERON TYPE I; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; JANUS KINASES; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; VARICELLOVIRUS;

EID: 84930341933     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004901     Document Type: Article

References (78)

1. Gilden D, Cohrs RJ, Mahalingam R, Nagel MA, Varicella zoster virus vasculopathies: diverse clinical manifestations, laboratory features, pathogenesis, and treatment. Lancet Neurol. 2009; 8: 731–740. doi: 10.1016/S1474-4422(09)70134-6 19608099
2. Matsunaga Y, Yamanishi K, Takahashi M, Experimental infection and immune response of guinea pigs with varicella-zoster virus. Infect Immun. 1982; 37: 407–412. 6288560
3. Wroblewska Z, Devlin M, Reilly K, van Trieste H, Wellish M, Gilden DH, The production of varicella Zoster virus antiserum in laboratory animals. Brief report. Arch Virol. 1982; 74: 233–238. 6299237
4. Gray WL, Simian varicella: a model for human varicella-zoster virus infections. Rev Med Virol. 2004; 14: 363–381. 15386593
5. Messaoudi I, Barron A, Wellish M, Engelmann F, Legasse A, Planer S, et al. Simian varicella virus infection of rhesus macaques recapitulates essential features of varicella zoster virus infection in humans. PLoS Pathog. 2009; 5: e1000657. doi: 10.1371/journal.ppat.1000657 19911054
6. Wang BX, Fish EN, The yin and yang of viruses and interferons. Trends Immunol. 2012; 33: 190–197. doi: 10.1016/j.it.2012.01.004 22321608
7. Levy DE, Garcia-Sastre A, The virus battles: IFN induction of the antiviral state and mechanisms of viral evasion. Cytokine Growth Factor Rev. 2001; 12: 143–156. 11325598
8. Wilkins C, Gale M, Jr.Recognition of viruses by cytoplasmic sensors. Curr Opin Immunol. 2010; 22: 41–47. doi: 10.1016/j.coi.2009.12.003 20061127
9. Seya T, Kasamatsu J, Azuma M, Shime H, Matsumoto M, Natural killer cell activation secondary to innate pattern sensing. J Innate Immun. 2011; 3: 264–273. doi: 10.1159/000326891 21454965
10. Le Bon A, Tough DF, Links between innate and adaptive immunity via type I interferon. Curr Opin Immunol. 2002; 14: 432–436. 12088676
11. Tovey MG, Lallemand C, Thyphronitis G, Adjuvant activity of type I interferons. Biol Chem. 2008; 389: 541–545. 18953720
12. Ku CC, Zerboni L, Ito H, Graham BS, Wallace M, Arvin AM, Varicella-zoster virus transfer to skin by T Cells and modulation of viral replication by epidermal cell interferon-alpha. J Exp Med. 2004; 200: 917–925. 15452178
13. Sen N, Sommer M, Che X, White K, Ruyechan WT, Arvin AM, Varicella-zoster virus immediate-early protein 62 blocks interferon regulatory factor 3 (IRF3) phosphorylation at key serine residues: a novel mechanism of IRF3 inhibition among herpesviruses. J Virol. 2010; 84: 9240–9253. doi: 10.1128/JVI.01147-10 20631144
14. Vandevenne P, Lebrun M, El Mjiyad N, Ote I, Di Valentin E, Habraken Y, et al. The varicella-zoster virus ORF47 kinase interferes with host innate immune response by inhibiting the activation of IRF3. PLoS One. 2011; 6: e16870. doi: 10.1371/journal.pone.0016870 21347389
15. Zhu H, Zheng C, Xing J, Wang S, Li S, Lin R, et al. Varicella-zoster virus immediate-early protein ORF61 abrogates the IRF3-mediated innate immune response through degradation of activated IRF3. J Virol. 2011; 85: 11079–11089. doi: 10.1128/JVI.05098-11 21835786
16. Sloan E, Henriquez R, Kinchington PR, Slobedman B, Abendroth A, Varicella-zoster virus inhibition of the NF-kappaB pathway during infection of human dendritic cells: role for open reading frame 61 as a modulator of NF-kappaB activity. J Virol. 2012; 86: 1193–1202. doi: 10.1128/JVI.06400-11 22090112
17. Ambagala AP, Cohen JI, Varicella-Zoster virus IE63, a major viral latency protein, is required to inhibit the alpha interferon-induced antiviral response. J Virol. 2007; 81: 7844–7851. 17507475
18. Shuai K, Liu B, Regulation of JAK-STAT signalling in the immune system. Nat Rev Immunol. 2003; 3: 900–911. 14668806
19. Davison AJ, Scott JE, The complete DNA sequence of varicella-zoster virus. J Gen Virol. 1986; 67 (Pt 9): 1759–1816. 3018124
20. Mueller NH, Walters MS, Marcus RA, Graf LL, Prenni J, Gilden D, et al. Identification of phosphorylated residues on varicella-zoster virus immediate-early protein ORF63. J Gen Virol. 2010; 91: 1133–1137. doi: 10.1099/vir.0.019067-0 20089801
21. Mahalingam R, Wellish M, Cohrs R, Debrus S, Piette J, Rentier B, et al. Expression of protein encoded by varicella-zoster virus open reading frame 63 in latently infected human ganglionic neurons. Proc Natl Acad Sci U S A. 1996; 93: 2122–2124. 8700895
22. Zerboni L, Sobel RA, Ramachandran V, Rajamani J, Ruyechan W, Abendroth A, et al. Expression of varicella-zoster virus immediate-early regulatory protein IE63 in neurons of latently infected human sensory ganglia. J Virol. 2010; 84: 3421–3430. doi: 10.1128/JVI.02416-09 20106930
23. Jackers P, Defechereux P, Baudoux L, Lambert C, Massaer M, Merville-Louis MP, et al. Characterization of regulatory functions of the varicella-zoster virus gene 63-encoded protein. J Virol. 1992; 66: 3899–3903. 1316489
24. Kost RG, Kupinsky H, Straus SE, Varicella-zoster virus gene 63: transcript mapping and regulatory activity. Virology. 1995; 209: 218–224. 7747473
25. Bontems S, Di Valentin E, Baudoux L, Rentier B, Sadzot-Delvaux C, Piette J, Phosphorylation of varicella-zoster virus IE63 protein by casein kinases influences its cellular localization and gene regulation activity. J Biol Chem. 2002; 277: 21050–21060. 11912195
26. Desloges N, Rahaus M, Wolff MH, The varicella-zoster virus-mediated delayed host shutoff: open reading frame 17 has no major function, whereas immediate-early 63 protein represses heterologous gene expression. Microbes Infect. 2005; 7: 1519–1529. 16039898
27. Hood C, Cunningham AL, Slobedman B, Arvin AM, Sommer MH, Kinchington PR, et al. Varicella-zoster virus ORF63 inhibits apoptosis of primary human neurons. J Virol. 2006; 80: 1025–1031. 16379003
28. Gray WL, Starnes B, White MW, Mahalingam R, The DNA sequence of the simian varicella virus genome. Virology. 2001; 284: 123–130. 11352673
29. Brazeau E, Wellish M, Kaufer BB, Tischer BK, Gray W, Zhou F, et al. Simian varicella virus open reading frame 63/70 expression is required for efficient virus replication in culture. J Neurovirol. 2011; 17: 274–280. doi: 10.1007/s13365-011-0025-6 21479719
30. Robinson BA, Estep RD, Messaoudi I, Rogers KS, Wong SW, Viral interferon regulatory factors decrease the induction of type I and type II interferon during rhesus macaque rhadinovirus infection. J Virol. 2012; 86: 2197–2211. doi: 10.1128/JVI.05047-11 22156526
31. Gierasch WW, Zimmerman DL, Ward SL, Vanheyningen TK, Romine JD, Leib DA, Construction and characterization of bacterial artificial chromosomes containing HSV-1 strains 17 and KOS. J Virol Methods. 2006; 135: 197–206. 16647145
32. DeFilippis VR, Sali T, Alvarado D, White L, Bresnahan W, Fruh KJ, Activation of the interferon response by human cytomegalovirus occurs via cytoplasmic double-stranded DNA but not glycoprotein B. J Virol. 2010; 84: 8913–8925. doi: 10.1128/JVI.00169-10 20573816
33. Mahalingam R, Wellish M, White T, Soike K, Cohrs R, Kleinschmidt-DeMasters BK, et al. Infectious simian varicella virus expressing the green fluorescent protein. J Neurovirol. 1998; 4: 438–444. 9718136
34. Eisfeld AJ, Yee MB, Erazo A, Abendroth A, Kinchington PR, Downregulation of class I major histocompatibility complex surface expression by varicella-zoster virus involves open reading frame 66 protein kinase-dependent and -independent mechanisms. J Virol. 2007; 81: 9034–9049. 17567702
35. Lenac Rovis T, Bailer SM, Pothineni VR, Ouwendijk WJ, Simic H, Babic M, et al. Comprehensive analysis of varicella-zoster virus proteins using a new monoclonal antibody collection. J Virol. 2013; 87: 6943–6954. doi: 10.1128/JVI.00407-13 23596286
36. Hardy S, Kitamura M, Harris-Stansil T, Dai Y, Phipps ML, Construction of adenovirus vectors through Cre-lox recombination. J Virol. 1997; 71: 1842–1849. 9032314
37. Gossen M, Bujard H, Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A. 1992; 89: 5547–5551. 1319065
38. Livak KJ, Schmittgen TD, Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25: 402–408. 11846609
39. Gray WL, Zhou F, Noffke J, Tischer BK, Cloning the simian varicella virus genome in E. coli as an infectious bacterial artificial chromosome. Arch Virol. 2011; 156: 739–746. doi: 10.1007/s00705-010-0889-4 21487663
40. Tischer BK, von Einem J, Kaufer B, Osterrieder N, Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques. 2006; 40: 191–197. 16526409
41. Gray WL, Mahalingam R, A cosmid-based system for inserting mutations and foreign genes into the simian varicella virus genome. J Virol Methods. 2005; 130: 89–94. 16043236
42. Reich NC, Liu L, Tracking STAT nuclear traffic. Nat Rev Immunol. 2006; 6: 602–612. 16868551
43. Erazo A, Kinchington PR, Varicella-zoster virus open reading frame 66 protein kinase and its relationship to alphaherpesvirus US3 kinases. Curr Top Microbiol Immunol. 2010; 342: 79–98. doi: 10.1007/82_2009_7 20186610
44. Kinchington PR, Fite K, Seman A, Turse SE, Virion association of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, requires expression of the VZV open reading frame 66 protein kinase. J Virol. 2001; 75: 9106–9113. 11533174
45. Mahalingam R, Gilden DH, Wellish M, Pugazhenthi S, Transactivation of the simian varicella virus (SVV) open reading frame (ORF) 21 promoter by SVV ORF 62 is upregulated in neuronal cells but downregulated in non-neuronal cells by SVV ORF 63 protein. Virology. 2006; 345: 244–250. 16242745
46. Leonard GT, Sen GC, Effects of adenovirus E1A protein on interferon-signaling. Virology. 1996; 224: 25–33. 8862396
47. Ivashkiv LB, Donlin LT, Regulation of type I interferon responses. Nat Rev Immunol. 2014; 14: 36–49. doi: 10.1038/nri3581 24362405
48. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity. 2000; 13: 539–548. 11070172
49. Yanai H, Chen HM, Inuzuka T, Kondo S, Mak TW, Takaoka A, et al. Role of IFN regulatory factor 5 transcription factor in antiviral immunity and tumor suppression. Proc Natl Acad Sci U S A. 2007; 104: 3402–3407. 17360658
50. Reid SP, Leung LW, Hartman AL, Martinez O, Shaw ML, Carbonnelle C, et al. Ebola virus VP24 binds karyopherin alpha1 and blocks STAT1 nuclear accumulation. J Virol. 2006; 80: 5156–5167. 16698996
51. Porritt RA, Hertzog PJ, Dynamic control of type I IFN signalling by an integrated network of negative regulators. Trends Immunol. 2015; 36: 150–160. doi: 10.1016/j.it.2015.02.002 25725583
52. Iwamoto M, Bjorklund T, Lundberg C, Kirik D, Wandless TJ, A general chemical method to regulate protein stability in the mammalian central nervous system. Chem Biol. 2010; 17: 981–988. doi: 10.1016/j.chembiol.2010.07.009 20851347
53. Nagel MA, James SF, Traktinskiy I, Wyborny A, Choe A, Rempel A, et al. Inhibition of pSTAT1 Nuclear Translocation and Antiviral Protein Expression in Human Brain Vascular Adventitial Fibroblasts Infected with Varicella Zoster Virus. J Virol. 2014.
54. Grinfeld E, Kennedy PG, Translation of varicella-zoster virus genes during human ganglionic latency. Virus Genes. 2004; 29: 317–319. 15550771
55. Kennedy PG, Grinfeld E, Bell JE, Varicella-zoster virus gene expression in latently infected and explanted human ganglia. J Virol. 2000; 74: 11893–11898. 11090189
56. Lungu O, Panagiotidis CA, Annunziato PW, Gershon AA, Silverstein SJ, Aberrant intracellular localization of Varicella-Zoster virus regulatory proteins during latency. Proc Natl Acad Sci U S A. 1998; 95: 7080–7085. 9618542
57. Arnold MM, Barro M, Patton JT, Rotavirus NSP1 mediates degradation of interferon regulatory factors through targeting of the dimerization domain. J Virol. 2013; 87: 9813–9821. doi: 10.1128/JVI.01146-13 23824805
58. Leonard GT, Sen GC, Restoration of interferon responses of adenovirus E1A-expressing HT1080 cell lines by overexpression of p48 protein. J Virol. 1997; 71: 5095–5101. 9188575
59. Graham FL, Smiley J, Russell WC, Nairn R, Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol. 1977; 36: 59–74. 886304
60. Haeussler DJ, Evangelista AM, Burgoyne JR, Cohen RA, Bachschmid MM, Pimental DR, Checkpoints in adenoviral production: cross-contamination and E1A. PLoS One. 2011; 6: e23160. doi: 10.1371/journal.pone.0023160 21826235
61. Zurney J, Kobayashi T, Holm GH, Dermody TS, Sherry B, Reovirus mu2 protein inhibits interferon signaling through a novel mechanism involving nuclear accumulation of interferon regulatory factor 9. J Virol. 2009; 83: 2178–2187. doi: 10.1128/JVI.01787-08 19109390
62. Barnard P, McMillan NA, The human papillomavirus E7 oncoprotein abrogates signaling mediated by interferon-alpha. Virology. 1999; 259: 305–313. 10388655
63. Banninger G, Reich NC, STAT2 nuclear trafficking. J Biol Chem. 2004; 279: 39199–39206. 15175343
64. Kimura T, Kadokawa Y, Harada H, Matsumoto M, Sato M, Kashiwazaki Y, et al. Essential and non-redundant roles of p48 (ISGF3 gamma) and IRF-1 in both type I and type II interferon responses, as revealed by gene targeting studies. Genes Cells. 1996; 1: 115–124. 9078371
65. Maiwald T, Schneider A, Busch H, Sahle S, Gretz N, Weiss TS, et al. Combining theoretical analysis and experimental data generation reveals IRF9 as a crucial factor for accelerating interferon alpha-induced early antiviral signalling. FEBS J. 2010; 277: 4741–4754. doi: 10.1111/j.1742-4658.2010.07880.x 20964804
66. Abendroth A, Slobedman B, Lee E, Mellins E, Wallace M, Arvin AM, Modulation of major histocompatibility class II protein expression by varicella-zoster virus. J Virol. 2000; 74: 1900–1907. 10644363
67. Gauzzi MC, Velazquez L, McKendry R, Mogensen KE, Fellous M, Pellegrini S, Interferon-alpha-dependent activation of Tyk2 requires phosphorylation of positive regulatory tyrosines by another kinase. J Biol Chem. 1996; 271: 20494–20500. 8702790
68. Muller M, Briscoe J, Laxton C, Guschin D, Ziemiecki A, Silvennoinen O, et al. The protein tyrosine kinase JAK1 complements defects in interferon-alpha/beta and -gamma signal transduction. Nature. 1993; 366: 129–135. 8232552
69. Zerboni L, Sen N, Oliver SL, Arvin AM, Molecular mechanisms of varicella zoster virus pathogenesis. Nat Rev Microbiol. 2014; 12: 197–210. doi: 10.1038/nrmicro3215 24509782
70. Mordstein M, Neugebauer E, Ditt V, Jessen B, Rieger T, Falcone V, et al. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J Virol. 2010; 84: 5670–5677. doi: 10.1128/JVI.00272-10 20335250
71. Pott J, Mahlakoiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, et al. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc Natl Acad Sci U S A. 2011; 108: 7944–7949. doi: 10.1073/pnas.1100552108 21518880
72. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR, Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol. 2006; 80: 4501–4509. 16611910
73. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE, et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol. 2003; 4: 63–68. 12469119
74. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, et al. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol. 2003; 4: 69–77. 12483210
75. Sommereyns C, Paul S, Staeheli P, Michiels T, IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 2008; 4: e1000017. doi: 10.1371/journal.ppat.1000017 18369468
76. Fuld S, Cunningham C, Klucher K, Davison AJ, Blackbourn DJ, Inhibition of interferon signaling by the Kaposi's sarcoma-associated herpesvirus full-length viral interferon regulatory factor 2 protein. J Virol. 2006; 80: 3092–3097. 16501120
77. Mutocheluh M, Hindle L, Areste C, Chanas SA, Butler LM, Lowry K, et al. Kaposi's sarcoma-associated herpesvirus viral interferon regulatory factor-2 inhibits type 1 interferon signalling by targeting interferon-stimulated gene factor-3. J Gen Virol. 2011; 92: 2394–2398. doi: 10.1099/vir.0.034322-0 21697347
78. Arvin AM, Kushner JH, Feldman S, Baehner RL, Hammond D, Merigan TC, Human leukocyte interferon for the treatment of varicella in children with cancer. N Engl J Med. 1982; 306: 761–765. 6174864