Differentiation of neurons restricts arbovirus replication and increases expression of the alpha isoform of IRF-7

Journal of Virology

Volumn 89, Issue 1, 2015, Pages 48-60

  Schultz, Kimberly L W ^a   Vernon, Patty S ^a,b   Griffin, Diane E ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b SCRIPPS MERCY HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; ISOPROTEIN; STAT1 PROTEIN; TRANSCRIPTION FACTOR; VIRUS PROTEIN; VIRUS RNA;

ANIMAL CELL; AP 7 CELL LINE; ARBOVIRUS; ARTICLE; CELL DEATH; CELL LINE; CELL MATURATION; GENE EXPRESSION; GENE SILENCING; IN VITRO STUDY; INFECTION SENSITIVITY; LA CROSSE VIRUS; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; OLFACTORY BULB; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RAT; RNA SYNTHESIS; SIGNAL TRANSDUCTION; SINDBIS VIRUS; TRANSLATION REGULATION; VENEZUELAN EQUINE ENCEPHALOMYELITIS ALPHAVIRUS; VIROGENESIS; VIRUS INHIBITION; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; GENE EXPRESSION PROFILING; IMMUNOLOGY; NERVE CELL; ORTHOBUNYAVIRUS; PHYSIOLOGY; VENEZUELAN EQUINE ENCEPHALITIS VIRUS; VIROLOGY;

ALPHAVIRUS; ARBOVIRUS; LA CROSSE VIRUS; MUS; RATTUS; SINDBIS VIRUS; VENEZUELAN EQUINE ENCEPHALITIS VIRUS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; ENCEPHALITIS VIRUS, VENEZUELAN EQUINE; GENE EXPRESSION PROFILING; INTERFERON REGULATORY FACTOR-7; MICE, INBRED C57BL; NEURONS; ORTHOBUNYAVIRUS; PROTEIN ISOFORMS; RATS; SINDBIS VIRUS; VIRUS REPLICATION;

EID: 84919459222     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02394-14     Document Type: Article

References (83)

1. Ben-Hur T, Hadar J, Shtram Y, Gilden DH, Becker Y. 1983. Neurovirulence of herpes simplex virus type 1 depends on age in mice and thymidine kinase expression. Arch Virol 78:303-308. http://dx.doi.org/10.1007/BF01311326.
2. Bennett RS, Cress CM, Ward JM, Firestone C-Y, Murphy BR, Whitehead SS. 2008. La Crosse virus infectivity, pathogenesis, and immunogenicity in mice and monkeys. Virol J 5:25. http://dx.doi.org/10.1186/1743-422X-5-25.
3. Ikegami H, Takeda M, Doi K. 1997. An age-related change in susceptibility of rat brain to encephalomyocarditis virus infection. Int J Exp Pathol 78:101-107.
4. Johnson RT, McFarland HF, Levy SE. 1972. Age-dependent resistance to viral encephalitis: studies of infections due to Sindbis virus in mice. J Infect Dis 125:257-262. http://dx.doi.org/10.1093/infdis/125.3.257.
5. McJunkin JE, de Los Reyes EC, Irazuzta JE, Caceres MJ, Khan RR, Minnich LL, Fu KD, Lovett GD, Tsai T, Thompson A. 2001. La Crosse encephalitis in children. N Engl J Med 344:801-807. http://dx.doi.org/10.1056/NEJM200103153441103.
6. McKendall RR, Woo W. 1987. Possible neural basis for age-dependent resistance to neurologic disease from herpes simplex virus. J Neurol Sci 81:227-237. http://dx.doi.org/10.1016/0022-510X(87)90098-0.
7. Sigel MM. 1952. Influence of age on susceptibility to virus infections with particular reference to laboratory animals. Annu Rev Microbiol 6:247-280. http://dx.doi.org/10.1146/annurev.mi.06.100152.001335.
8. Taguchi F, Aiuchi M, Fujiwara K. 1977. Age-dependent response of mice to a mouse hepatitis virus, MHV-S. Jpn J Exp Med 47:109-115.
9. Tardieu M, Powers ML, Weiner HL. 1983. Age dependent susceptibility to reovirus type 3 encephalitis: role of viral and host factors. Ann Neurol 13:602-607. http://dx.doi.org/10.1002/ana.410130604.
10. Griffin DE. 1976. Role of the immune response in age-dependent resistance of mice to encephalitis due to Sindbis virus. J Infect Dis 133:456-464. http://dx.doi.org/10.1093/infdis/133.4.456.
11. Oliver KR, Scallan MF, Dyson H, Fazakerley JK. 1997. Susceptibility to a neurotropic virus and its changing distribution in the developing brain is a function of CNS maturity. J Neurovirol 3:38-48. http://dx.doi.org/10.3109/13550289709015791.
12. Kunin CM. 1962. Virus-tissue union and the pathogenesis of enterovirus infections. J Immunol 88:556-569.
13. Labrada L, Liang XH, Zheng W, Johnston C, Levine B. 2002. Agedependent resistance to lethal alphavirus encephalitis in mice: analysis of gene expression in the central nervous system and identification of a novel interferon-inducible protective gene, mouse ISG12. J Virol 76:11688-11703. http://dx.doi.org/10.1128/JVI.76.22.11688-11703.2002.
14. Ubol S, Griffin DE. 1991. Identification of a putative alphavirus receptor on mouse neural cells. J Virol 65:6913-6921.
15. Vernon PS, Griffin DE. 2005. Characterization of an in vitro model of alphavirus infection of immature and mature neurons. J Virol 79:3438-3447. http://dx.doi.org/10.1128/JVI.79.6.3438-3447.2005.
16. Binder GK, Griffin DE. 2003. Immune-mediated clearance of virus from the central nervous system. Microbes Infect 5:439-448. http://dx.doi.org/10.1016/S1286-4579(03)00047-9.
17. Chakraborty S, Kaushik DK, Gupta M, Basu A. 2010. Inflammasome signaling at the heart of central nervous system pathology. J Neurosci Res 88:1615-1631. http://dx.doi.org/10.1002/jnr.22343.
18. Maher SG, Romero-Weaver AL, Scarzello AJ, Gamero AM. 2007. Interferon: cellular executioner or white knight?. Curr Med Chem 14:1279-1289. http://dx.doi.org/10.2174/092986707780597907.
19. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47. http://dx.doi.org/10.1099/vir.0.83391-0.
20. Després P, Griffin JW, Griffin DE. 1995. Antiviral activity of alpha interferon in Sindbis virus-infected cells is restored by anti-E2 monoclonal antibody treatment. J Virol 69:7345-7348.
21. Byrnes AP, Durbin JE, Griffin DE. 2000. Control of Sindbis virus infection by antibody in interferon-deficient mice. J Virol 74:3905-3908. http://dx.doi.org/10.1128/JVI.74.8.3905-3908.2000.
22. Müller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921. http://dx.doi.org/10.1126/science.8009221.
23. Frolov I, Akhrymuk M, Akhrymuk I, Atasheva S, Frolova EI. 2012. Early events in alphavirus replication determine the outcome of infection. J Virol 86:5055-5066. http://dx.doi.org/10.1128/JVI.07223-11.
24. Ryman KD, Klimstra WB, Nguyen KB, Biron CA, Johnston RE. 2000. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J Virol 74:3366-3378. http://dx.doi.org/10.1128/JVI.74.7.3366-3378.2000.
25. Kinney RM, Chang GJ, Tsuchiya KR, Sneider JM, Roehrig JT, Woodward TM, Trent DW. 1993. Attenuation of Venezuelan equine encephalitis virus strain TC-83 is encoded by the 5'-noncoding region and the E2 envelope glycoprotein. J Virol 67:1269-1277.
26. White LJ, Wang JG, Davis NL, Johnston RE. 2001. Role of alpha/beta interferon in Venezuelan equine encephalitis virus pathogenesis: effect of an attenuating mutation in the 5' untranslated region. J Virol 75:3706-3718. http://dx.doi.org/10.1128/JVI.75.8.3706-3718.2001.
27. Blakqori G, Delhaye S, Habjan M, Blair CD, Sánchez-Vargas I, Olson KE, Attarzadeh-Yazdi G, Fragkoudis R, Kohl A, Kalinke U, Weiss S, Michiels T, Staeheli P, Weber F. 2007. La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol 81:4991-4999. http://dx.doi.org/10.1128/JVI.01933-06.
28. Delhaye S, Paul S, Blakqori G, Minet M, Weber F, Staeheli P, Michiels T. 2006. Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci USA 103:7835-7840. http://dx.doi.org/10.1073/pnas.0602460103.
29. Lienenklaus S, Cornitescu M, Zietara N, Lyszkiewicz M, Gekara N, Jablónska J, Edenhofer F, Rajewsky K, Bruder D, Hafner M, Staeheli P, Weiss S. 2009. Novel reporter mouse reveals constitutive and inflammatory expression of IFN-beta in vivo. J Immunol 183:3229-3236. http://dx.doi.org/10.4049/jimmunol.0804277.
30. Dionne KR, Galvin JM, Schittone SA, Clarke P, Tyler KL. 2011. Type I interferon signaling limits reoviral tropism within the brain and prevents lethal systemic infection. J Neurovirol 17:314-326. http://dx.doi.org/10.1007/s13365-011-0038-1.
31. Chopy D, Detje CN, Lafage M, Kalinke U, Lafon M. 2011. The type I interferon response bridles rabies virus infection and reduces pathogenicity. J Neurovirol 17:353-367. http://dx.doi.org/10.1007/s13365-011-0041-6.
32. Préhaud C, Mégret F, Lafage M, Lafon M. 2005. Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol 79:12893-12904. http://dx.doi.org/10.1128/JVI.79.20.12893-12904.2005.
33. Castorena KM, Peltier DC, Peng W, Miller DJ. 2008. Maturationdependent responses of human neuronal cells to western equine encephalitis virus infection and type I interferons. Virology 372:208-220. http://dx.doi.org/10.1016/j.virol.2007.10.025.
34. Farmer JR, Altschaefl KM, O'Shea KS, Miller DJ. 2013. Activation of the type I interferon pathway is enhanced in response to human neuronal differentiation. PLoS One 8:e58813. http://dx.doi.org/10.1371/journal.pone.0058813.
35. Kato H, Takahasi K, Fujita T. 2011. RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol Rev 243:91-98. http://dx.doi.org/10.1111/j.1600-065X.2011.01052.x.
36. Levy DE, Marié IJ. 2004. RIGging an antiviral defense: it's in the CARDs. Nat Immunol 5:699-701. http://dx.doi.org/10.1038/ni0704-699.
37. Taniguchi T, Takaoka A. 2001. A weak signal for strong responses: interferon-alpha/beta revisited. Nat Rev Mol Cell Biol 2:378-386. http://dx.doi.org/10.1038/35073080.
38. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N, Goodbourn S, Randall RE. 2004. The V proteins of paramyxoviruses bind the IFNinducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci USA 101:17264-17269. http://dx.doi.org/10.1073/pnas.0407639101.
39. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5:730-737. http://dx.doi.org/10.1038/ni1087.
40. Barnes BJ. 2003. Virus-induced heterodimer formation between IRF-5 and IRF-7 modulates assembly of the IFNA enhanceosome in vivo and transcriptional activity of IFNA genes. J Biol Chem 278:16630-16641. http://dx.doi.org/10.1074/jbc.M212609200.
41. Juang YT, Lowther W, Kellum M, Au WC, Lin R, Hiscott J, Pitha PM. 1998. Primary activation of interferon A and interferon B gene transcription by interferon regulatory factor 3. Proc Natl Acad Sci USA 95:9837-9842. http://dx.doi.org/10.1073/pnas.95.17.9837.
42. Au WC, Moore PA, LaFleur DW, Tombal B, Pitha PM. 1998. Characterization of the interferon regulatory factor-7 and its potential role in the transcription activation of interferon A genes. J Biol Chem 273:29210-29217. http://dx.doi.org/10.1074/jbc.273.44.29210.
43. Marié I, Durbin JE, Levy DE. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J 17:6660-6669. http://dx.doi.org/10.1093/emboj/17.22.6660.
44. Schilte C, Buckwalter MR, Laird ME, Diamond MS, Schwartz O, Albert ML. 2012. Cutting edge: independent roles for IRF-3 and IRF-7 in hematopoietic and nonhematopoietic cells during host response to Chikungunya infection. J Immunol 188:2967-2971. http://dx.doi.org/10.4049/jimmunol.1103185.
45. Daffis S, Samuel MA, Keller BC, Gale M, Diamond MS. 2007. Cellspecific IRF-3 responses protect against West Nile virus infection by interferon-dependent and-independent mechanisms. PLoS Pathog 3:e106. http://dx.doi.org/10.1371/journal.ppat.0030106.
46. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, Nakaya T, Katsuki M, Noguchi S, Tanaka N, Taniguchi T. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13:539-548. http://dx.doi.org/10.1016/S1074-7613(00)00053-4.
47. Honda K, Yanai H, Negishi H, Asagiri M, Sato M, Mizutani T, Shimada N, Ohba Y, Takaoka A, Yoshida N, Taniguchi T. 2005. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434:772-777. http://dx.doi.org/10.1038/nature03464.
48. Bego MG, Mercier J, Cohen EA. 2012. Virus-activated interferon regulatory factor 7 upregulates expression of the interferon-regulated BST2 gene independently of interferon signaling. J Virol 86:3513-3527. http://dx.doi.org/10.1128/JVI.06971-11.
49. Peltier DC, Lazear HM, Farmer JR, Diamond MS, Miller DJ. 2013. Neurotropic arboviruses induce interferon regulatory factor 3-mediated neuronal responses that are cytoprotective, interferon independent, and inhibited by Western equine encephalitis virus capsid. J Virol 87:1821-1833. http://dx.doi.org/10.1128/JVI.02858-12.
50. Murrell JR, Hunter DD. 1999. An olfactory sensory neuron line, odora, properly targets olfactory proteins and responds to odorants. J Neurosci 19:8260-8270.
51. Kerr DA, Lladó J, Shamblott MJ, Maragakis NJ, Irani DN, Crawford TO, Krishnan C, Dike S, Gearhart JD, Rothstein JD. 2003. Human embryonic germ cell derivatives facilitate motor recovery of rats with diffuse motor neuron injury. J Neurosci 23:5131-5140.
52. Levine B, Huang Q, Isaacs JT, Reed JC, Griffin DE. 1993. Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 361:739-742. http://dx.doi.org/10.1038/361739a0.
53. Lustig S, Jackson AC, Hahn CS, Griffin DE, Strauss EG, Strauss JH. 1988. Molecular basis of Sindbis virus neurovirulence in mice. J Virol 62:2329-2336.
54. Janssen R, Gonzalez-Scarano F. 1984. Mechanisms of bunyavirus virulence. Comparative pathogenesis of a virulent strain of La Crosse and an avirulent strain of Tahyna virus. Lab Invest 50:447-455.
55. Stanley J, Cooper SJ, Griffin DE. 1985. Alphavirus neurovirulence: monoclonal antibodies discriminating wild-type from neuroadapted Sindbis virus. J Virol 56:110-119.
56. Roehrig JT, Mathews JH. 1985. The neutralization site on the E2 glycoprotein of Venezuelan equine encephalomyelitis (TC-83) virus is composed of multiple conformationally stable epitopes. Virology 142:347-356. http://dx.doi.org/10.1016/0042-6822(85)90343-5.
57. Park E, Griffin DE. 2009. Interaction of Sindbis virus non-structural protein 3 with poly(ADP-ribose) polymerase 1 in neuronal cells. J Gen Virol 90:2073-2080. http://dx.doi.org/10.1099/vir.0.012682-0.
58. Levine B, Goldman JE, Jiang HH, Griffin DE, Hardwick JM. 1996. Bc1-2 protects mice against fatal alphavirus encephalitis. Proc Natl Acad Sci U S A 93:4810-4815. http://dx.doi.org/10.1073/pnas.93.10.4810.
59. Lewis J, Wesselingh SL, Griffin DE, Hardwick JM. 1996. Alphavirusinduced apoptosis in mouse brains correlates with neurovirulence. J Virol 70:1828-1835.
60. Nava VE, Rosen A, Veliuona MA, Clem RJ, Levine B, Hardwick JM. 1998. Sindbis virus induces apoptosis through a caspase-dependent, CrmA-sensitive pathway. J Virol 72:452-459.
61. Ubol S, Park S, Budihardjo I, Desnoyers S, Montrose MH, Poirier GG, Kaufmann SH, Griffin DE. 1996. Temporal changes in chromatin, intracellular calcium, and poly(ADP-ribose) polymerase during Sindbis virusinduced apoptosis of neuroblastoma cells. J Virol 70:2215-2220.
62. Burdeinick-Kerr R, Govindarajan D, Griffin DE. 2009. Noncytolytic clearance of Sindbis virus infection from neurons by gamma interferon is dependent on Jak/Stat signaling. J Virol 83:3429-3435. http://dx.doi.org/10.1128/JVI.02381-08.
63. Marié I, Smith E, Prakash A, Levy DE. 2000. Phosphorylation-induced dimerization of interferon regulatory factor 7 unmasks DNA binding and a bipartite transactivation domain. Mol Cell Biol 20:8803-8814. http://dx.doi.org/10.1128/MCB.20.23.8803-8814.2000.
64. Prakash A, Levy DE. 2006. Regulation of IRF7 through cell type-specific protein stability. Biochem Biophys Res Commun 342:50-56. http://dx.doi.org/10.1016/j.bbrc.2006.01.122.
65. Hollidge BS, Weiss SR, Soldan SS. 2011. The role of interferon antagonist, non-structural proteins in the pathogenesis and emergence of arboviruses. Viruses 3:629-658. http://dx.doi.org/10.3390/v3060629.
66. Gorchakov R, Frolova E, Frolov I. 2005. Inhibition of transcription and translation in Sindbis virus-infected cells. J Virol 79:9397-9409. http://dx.doi.org/10.1128/JVI.79.15.9397-9409.2005.
67. Garmashova N, Atasheva S, Kang W, Weaver SC, Frolova E, Frolov I. 2007. Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J Virol 81:13552-13565. http://dx.doi.org/10.1128/JVI.01576-07.
68. Garmashova N, Gorchakov R, Volkova E, Paessler S, Frolova E, Frolov I. 2007. The Old World and New World alphaviruses use different virusspecific proteins for induction of transcriptional shutoff. J Virol 81:2472-2484. http://dx.doi.org/10.1128/JVI.02073-06.
69. Verbruggen P, Ruf M, Blakqori G, Overby AK, Heidemann M, Eick D, Weber F. 2011. Interferon antagonist NSs of La Crosse virus triggers a DNA damage response-like degradation of transcribing RNA polymerase II. J Biol Chem 286:3681-3692. http://dx.doi.org/10.1074/jbc.M110.154799.
70. Yin J, Gardner CL, Burke CW, Ryman KD, Klimstra WB. 2009. Similarities and differences in antagonism of neuron alpha/beta interferon responses by Venezuelan equine encephalitis and Sindbis alphaviruses. J Virol 83:10036-10047. http://dx.doi.org/10.1128/JVI.01209-09.
71. Hefti HP, Frese M, Landis H, Di Paolo C, Aguzzi A, Haller O, Pavlovic J. 1999. Human MxA protein protects mice lacking a functional alpha/beta interferon system against La crosse virus and other lethal viral infections. J Virol 73:6984-6991.
72. Christensen JE, Fenger C, Issazadeh-Navikas S, Krug A, Liljestrøm P, Goriely S, Paludan SR, Finsen B, Christensen JP, Thomsen AR. 2012. Differential impact of interferon regulatory factor 7 in initiation of the type I interferon response in the lymphocytic choriomeningitis virusinfected central nervous system versus the periphery. J Virol 86:7384-7392. http://dx.doi.org/10.1128/JVI.07090-11.
73. Suthar MS, Brassil MM, Blahnik G, McMillan A, Ramos HJ, Proll SC, Belisle SE, Katze MG, Gale M. 2013. A systems biology approach reveals that tissue tropism to West Nile virus is regulated by antiviral genes and innate immune cellular processes. PLoS Pathog 9:e1003168. http://dx.doi.org/10.1371/journal.ppat.1003168.
74. Clarke P, Leser JS, Bowen RA, Tyler KL. 2014. Virus-induced transcriptional changes in the brain include the differential expression of genes associated with interferon, apoptosis, interleukin 17 receptor A, and glutamate signaling as well as flavivirus-specific upregulation of tRNA synthetases. mBio 5(2):e00902-14. http://dx.doi.org/10.1128/mBio.00902-14.
75. Fensterl V, Wetzel JL, Ramachandran S, Ogino T, Stohlman SA, Bergmann CC, Diamond MS, Virgin HW, Sen GC. 2012. Interferon-induced Ifit2/ISG54 protects mice from lethal VSV neuropathogenesis. PLoS Pathog 8:e1002712. http://dx.doi.org/10.1371/journal.ppat.1002712.
76. Colina R, Costa-Mattioli M, Dowling RJO, Jaramillo M, Tai L-H, Breitbach CJ, Martineau Y, Larsson O, Rong L, Svitkin YV, Makrigiannis AP, Bell JC, Sonenberg N. 2008. Translational control of the innate immune response through IRF-7. Nature 452:323-328. http://dx.doi.org/10.1038/nature06730.
77. Esen N, Blakely PK, Rainey-Barger EK, Irani DN. 2012. Complexity of the microglial activation pathways that drive innate host responses during lethal alphavirus encephalitis in mice. ASN Neuro 4:207-221. http://dx.doi.org/10.1042/AN20120016.
78. Daffis S, Samuel MA, Suthar MS, Keller BC, Gale M, Diamond MS. 2008. Interferon regulatory factor IRF-7 induces the antiviral alpha interferon response and protects against lethal West Nile virus infection. J Virol 82:8465-8475. http://dx.doi.org/10.1128/JVI.00918-08.
79. Bandyopadhyay SK, Leonard GT, Bandyopadhyay T, Stark GR, Sen GC. 1995. Transcriptional induction by double-stranded RNA is mediated by interferon-stimulated response elements without activation of interferon-stimulated gene factor 3. J Biol Chem 270:19624-19629. http://dx.doi.org/10.1074/jbc.270.33.19624.
80. Di Domizio J, Blum A, Gallagher-Gambarelli M, Molens J-P, Chaperot L, Plumas J. 2009. TLR7 stimulation in human plasmacytoid dendritic cells leads to the induction of early IFN-inducible genes in the absence of type I IFN. Blood 114:1794-1802. http://dx.doi.org/10.1182/blood-2009-04-216770.
81. Lin R, Noyce RS, Collins SE, Everett RD, Mossman KL. 2004. The herpes simplex virus ICP0 RING finger domain inhibits IRF3-and IRF7-mediated activation of interferon-stimulated genes. J Virol 78:1675-1684. http://dx.doi.org/10.1128/JVI.78.4.1675-1684.2004.
82. Ning S, Huye LE, Pagano JS. 2005. Regulation of the transcriptional activity of the IRF7 promoter by a pathway independent of interferon signaling. J Biol Chem 280:12262-12270. http://dx.doi.org/10.1074/jbc.M404260200.
83. O'Donnell LA, Conway S, Rose RW, Nicolas E, Slifker M, Balachandran S, Rall GF. 2012. STAT1-independent control of a neurotropic measles virus challenge in primary neurons and infected mice. J Immunol 188: 1915-1923. http://dx.doi.org/10.4049/jimmunol.1101356.