Fast type I interferon response protects astrocytes from flavivirus infection and virus-induced cytopathic effects

Journal of Neuroinflammation

Volumn 13, Issue 1, 2016, Pages

  Lindqvist, Richard ^a,b   Mundt, Filip ^c   Gilthorpe, Jonathan D ^a   Wölfel, Silke ^d   Gekara, Nelson O ^a   Kröger, Andrea ^e,f   Överby, Anna K ^a,b  

^a UMEÅ UNIVERSITY   (Sweden)

^b Molecular Infection Medicine Sweden (MIMS)   (Sweden)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^d BUNDESWEHR INSTITUTE OF MICROBIOLOGY   (Germany)

^e HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^f OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Astrocytes; Flavivirus; Interferon; TBEV; Viperin

Indexed keywords

ALPHA INTERFERON RECEPTOR; INTERFERON; INTERFERON STIMULATED GENE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; ANTIVIRUS AGENT; IMMUNOGLOBULIN G; MESSENGER RNA; OXAZINE DERIVATIVE; RESAZURIN; XANTHENE DERIVATIVE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BIOINFORMATICS; CELL PROTECTION; CELL VIABILITY; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; EMBRYO; EVALUATION STUDY; FIBROBLAST; FLAVIVIRUS INFECTION; GENE EXPRESSION; IMMUNE RESPONSE; INNATE IMMUNITY; JAPANESE ENCEPHALITIS VIRUS; MOUSE; NERVE CELL; NONHUMAN; PROTEIN EXPRESSION; RNA SEQUENCE; SIGNAL TRANSDUCTION; TICK BORNE ENCEPHALITIS VIRUS; TRANSCRIPTION REGULATION; UPREGULATION; VIROGENESIS; VIRUS INDUCTION; VIRUS REPLICATION; VIRUS STRAIN; WEST NILE VIRUS; WILD TYPE; ZIKA VIRUS; ANIMAL; BIOLOGY; C57BL MOUSE; DRUG EFFECTS; FLAVIVIRUS; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; MALE; METABOLISM; NEWBORN; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

ANIMALS; ANIMALS, NEWBORN; ANTIVIRAL AGENTS; ASTROCYTES; COMPUTATIONAL BIOLOGY; FLAVIVIRUS; GENE EXPRESSION REGULATION, VIRAL; IMMUNOGLOBULIN G; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURONS; OXAZINES; RECEPTOR, INTERFERON ALPHA-BETA; RNA, MESSENGER; XANTHENES;

EID: 84992386988     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/s12974-016-0748-7     Document Type: Article

References (86)

1. Mansfield KL, Johnson N, Phipps LP, Stephenson JR, Fooks AR, Solomon T. Tick-borne encephalitis virus-a review of an emerging zoonosis. J Gen Virol. 2009;90:1781-94.
2. Dumpis U, Crook D, Oksi J. Tick-borne encephalitis. Clin Infect Dis. 1999;28:882-90.
3. Beasley DW. Vaccines and immunotherapeutics for the prevention and treatment of infections with West Nile virus. Immunotherapy. 2011;3:269-85.
4. Diamond MS. Progress on the development of therapeutics against West Nile virus. Antiviral Res. 2009;83:214-27.
5. Bossi P, Tegnell A, Baka A, Van Loock F, Hendriks J, Werner A, Maidhof H, Gouvras G, Task Force on b, Chemial Agent Threats PHDECL. Bichat guidelines for the clinical management of viral encephalitis and bioterrorism-related viral encephalitis. Euro Surveill. 2004;9:E21-2.
6. Tiroumourougane SV, Raghava P, Srinivasan S. Japanese viral encephalitis. Postgrad Med J. 2002;78:205-15.
7. Stetson DB, Medzhitov R. Type I interferons in host defense. Immunity. 2006;25:373-81.
8. Takeuchi O, Akira S. Innate immunity to virus infection. Immunol Rev. 2009;227:75-86.
9. Gonzalez-Navajas JM, Lee J, David M, Raz E. Immunomodulatory functions of type I interferons. Nat Rev Immunol. 2012;12:125-35.
10. Platanias LC. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat Rev Immunol. 2005;5:375-86.
11. Weber E, Finsterbusch K, Lindquist R, Nair S, Lienenklaus S, Gekara NO, Janik D, Weiss S, Kalinke U, Overby AK, Kroger A. Type I interferon protects mice from fatal neurotropic infection with Langat virus by systemic and local antiviral responses. J Virol. 2014;88:12202-12.
12. Lazear HM, Pinto AK, Vogt MR, Gale Jr M, Diamond MS. Beta interferon controls West Nile virus infection and pathogenesis in mice. J Virol. 2011;85:7186-94.
13. Samuel MA, Diamond MS. Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol. 2005;79:13350-61.
14. Aoki K, Shimada S, Simantini DS, Tun MM, Buerano CC, Morita K, Hayasaka D. Type-I interferon response affects an inoculation dose-independent mortality in mice following Japanese encephalitis virus infection. Virol J. 2014;11:105.
15. Lazear HM, Govero J, Smith AM, Platt DJ, Fernandez E, Miner JJ, Diamond MS. A mouse model of Zika virus pathogenesis. Cell Host Microbe. 2016;19:720-30.
16. Harris MG, Hulseberg P, Ling C, Karman J, Clarkson BD, Harding JS, Zhang M, Sandor A, Christensen K, Nagy A, et al. Immune privilege of the CNS is not the consequence of limited antigen sampling. Sci Rep. 2014;4:4422.
17. Nair S, Michaelsen-Preusse K, Finsterbusch K, Stegemann-Koniszewski S, Bruder D, Grashoff M, Korte M, Koster M, Kalinke U, Hauser H, Kroger A. Interferon regulatory factor-1 protects from fatal neurotropic infection with vesicular stomatitis virus by specific inhibition of viral replication in neurons. PLoS Pathog. 2014;10, e1003999.
18. Detje CN, Lienenklaus S, Chhatbar C, Spanier J, Prajeeth CK, Soldner C, Tovey MG, Schluter D, Weiss S, Stangel M, Kalinke U. Upon intranasal vesicular stomatitis virus infection, astrocytes in the olfactory bulb are important interferon beta producers that protect from lethal encephalitis. J Virol. 2015;89:2731-8.
19. Cho H, Proll SC, Szretter KJ, Katze MG, Gale Jr M, Diamond MS. Differential innate immune response programs in neuronal subtypes determine susceptibility to infection in the brain by positive-stranded RNA viruses. Nat Med. 2013;19:458-64.
20. Gelpi E, Preusser M, Garzuly F, Holzmann H, Heinz FX, Budka H. Visualization of Central European tick-borne encephalitis infection in fatal human cases. J Neuropathol Exp Neurol. 2005;64:506-12.
21. Cho H, Shrestha B, Sen GC, Diamond MS. A role for Ifit2 in restricting West Nile virus infection in the brain. J Virol. 2013;87:8363-71.
22. Reinert LS, Harder L, Holm CK, Iversen MB, Horan KA, Dagnaes-Hansen F, Ulhoi BP, Holm TH, Mogensen TH, Owens T, et al. TLR3 deficiency renders astrocytes permissive to herpes simplex virus infection and facilitates establishment of CNS infection in mice. J Clin Invest. 2012;122:1368-76.
23. Kallfass C, Ackerman A, Lienenklaus S, Weiss S, Heimrich B, Staeheli P. Visualizing production of beta interferon by astrocytes and microglia in brain of La Crosse virus-infected mice. J Virol. 2012;86:11223-30.
24. Lothman EW, Somjen GG. Extracellular potassium activity, intracellular and extracellular potential responses in the spinal cord. J Physiol. 1975;252:115-36.
25. Kimelberg HK, Biddlecome S, Bourke RS. SITS-inhibitable Cl- transport and Na+-dependent H+ production in primary astroglial cultures. Brain Res. 1979;173:111-24.
26. Martinez-Hernandez A, Bell KP, Norenberg MD. Glutamine synthetase: glial localization in brain. Science. 1977;195:1356-8.
27. Aschner M. Neuron-astrocyte interactions: implications for cellular energetics and antioxidant levels. Neurotoxicology. 2000;21:1101-7.
28. Farina C, Aloisi F, Meinl E. Astrocytes are active players in cerebral innate immunity. Trends Immunol. 2007;28:138-45.
29. Kornyey S. Contribution to the histology of tick-borne encephalitis. Acta Neuropathol. 1978;43:179-83.
30. German AC, Myint KS, Mai NT, Pomeroy I, Phu NH, Tzartos J, Winter P, Collett J, Farrar J, Barrett A, et al. A preliminary neuropathological study of Japanese encephalitis in humans and a mouse model. Trans R Soc Trop Med Hyg. 2006;100:1135-45.
31. van Marle G, Antony J, Ostermann H, Dunham C, Hunt T, Halliday W, Maingat F, Urbanowski MD, Hobman T, Peeling J, Power C. West Nile virus-induced neuroinflammation: glial infection and capsid protein-mediated neurovirulence. J Virol. 2007;81:10933-49.
32. Sips GJ, Wilschut J, Smit JM. Neuroinvasive flavivirus infections. Rev Med Virol. 2012;22:69-87.
33. Kurhade C, Zegenhagen L, Weber E, Nair S, Michaelsen-Preusse K, Spanier J, Gekara NO, Kroger A, Overby AK. Type I interferon response in olfactory bulb, the site of tick-borne flavivirus accumulation, is primarily regulated by IPS-1. J Neuroinflammation. 2016;13:22.
34. Palus M, Bily T, Elsterova J, Langhansova H, Salat J, Vancova M, Ruzek D. Infection and injury of human astrocytes by tick-borne encephalitis virus. J Gen Virol. 2014;95:2411-26.
35. Potokar M, Korva M, Jorgacevski J, Avsic-Zupanc T, Zorec R. Tick-borne encephalitis virus infects rat astrocytes but does not affect their viability. PLoS One. 2014;9, e86219.
36. Hussmann KL, Samuel MA, Kim KS, Diamond MS, Fredericksen BL. Differential replication of pathogenic and nonpathogenic strains of West Nile virus within astrocytes. J Virol. 2013;87:2814-22.
37. Diniz JA, Da Rosa AP, Guzman H, Xu F, Xiao SY, Popov VL, Vasconcelos PF, Tesh RB. West Nile virus infection of primary mouse neuronal and neuroglial cells: the role of astrocytes in chronic infection. Am J Trop Med Hyg. 2006;75:691-6.
38. Lucas M, Frenkiel MP, Mashimo T, Guenet JL, Deubel V, Despres P, Ceccaldi PE. The Israeli strain IS-98-ST1 of West Nile virus as viral model for West Nile encephalitis in the Old World. Virol J. 2004;1:9.
39. Chang CY, Li JR, Chen WY, Ou YC, Lai CY, Hu YH, Wu CC, Chang CJ, Chen CJ. Disruption of in vitro endothelial barrier integrity by Japanese encephalitis virus-infected astrocytes. Glia. 2015;63:1915-932.
40. Schildge S, Bohrer C, Beck K, Schachtrup C. Isolation and culture of mouse cortical astrocytes. J Vis Exp. 2013;e50079:1-7.
41. Dunning CJ, McGauran G, Willen K, Gouras GK, O'Connell DJ, Linse S. Direct high affinity interaction between Abeta42 and GSK3alpha stimulates hyperphosphorylation of tau. A new molecular link in Alzheimer's disease? ACS Chem Neurosci. 2016;7:161-70.
42. Overby AK, Popov VL, Niedrig M, Weber F. Tick-borne encephalitis virus delays interferon induction and hides its double-stranded RNA in intracellular membrane vesicles. J Virol. 2010;84:8470-83.
43. Schwaiger M, Cassinotti P. Development of a quantitative real-time RT-PCR assay with internal control for the laboratory detection of tick borne encephalitis virus (TBEV) RNA. J Clin Virol. 2003;27:136-45.
44. Niedrig M, Klockmann U, Lang W, Roeder J, Burk S, Modrow S, Pauli G. Monoclonal antibodies directed against tick-borne encephalitis virus with neutralizing activity in vivo. Acta Virol. 1994;38:141-9.
45. Cargnelutti JF, Brum MC, Weiblen R, Flores EF. Stable expression and potential use of West Nile virus envelope glycoproteins preM/E as antigen in diagnostic tests. Braz J Microbiol. 2011;42:1161-6.
46. Yousef H, Conboy MJ, Morgenthaler A, Schlesinger C, Bugaj L, Paliwal P, Greer C, Conboy IM, Schaffer D. Systemic attenuation of the TGF-beta pathway by a single drug simultaneously rejuvenates hippocampal neurogenesis and myogenesis in the same old mammal. Oncotarget. 2015;6:11959-78.
47. Perler L, Pfister H, Schweizer M, Peterhans E, Jungi TW. A bioassay for interferon type I based on inhibition of Sendai virus growth. J Immunol Methods. 1999;222:189-96.
48. Barrett AD, Hunt N, Dimmock NJ. A rapid method for the inactivation of virus infectivity prior to assay for interferons. J Virol Methods. 1984;8:349-51.
49. Horisberger MA, de Staritzky K. A recombinant human interferon-alpha B/D hybrid with a broad host-range. J Gen Virol. 1987;68(Pt 3):945-8.
50. Upadhyay AS, Vonderstein K, Pichlmair A, Stehling O, Bennett KL, Dobler G, Guo JT, Superti-Furga G, Lill R, Overby AK, Weber F. Viperin is an iron-sulfur protein that inhibits genome synthesis of tick-borne encephalitis virus via radical SAM domain activity. Cell Microbiol. 2014;16:834-48.
51. Clarke P, Leser JS, Quick ED, Dionne KR, Beckham JD, Tyler KL. Death receptor-mediated apoptotic signaling is activated in the brain following infection with West Nile virus in the absence of a peripheral immune response. J Virol. 2014;88:1080-9.
52. Kolokoltsova OA, Yun NE, Paessler S. Reactive astrogliosis in response to hemorrhagic fever virus: microarray profile of Junin virus-infected human astrocytes. Virol J. 2014;11:126.
53. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102:15545-50.
54. Lamb J, Crawford ED, Peck D, Modell JW, Blat IC, Wrobel MJ, Lerner J, Brunet JP, Subramanian A, Ross KN, et al. The connectivity map: using gene-expression signatures to connect small molecules, genes, and disease. Science. 2006;313:1929-35.
55. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7:562-78.
56. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28:511-5.
57. Gritsun TS, Frolova TV, Zhankov AI, Armesto M, Turner SL, Frolova MP, Pogodina VV, Lashkevich VA, Gould EA. Characterization of a Siberian virus isolated from a patient with progressive chronic tick-borne encephalitis. J Virol. 2003;77:25-36.
58. Dorrbecker B, Dobler G, Spiegel M, Hufert FT. Tick-borne encephalitis virus and the immune response of the mammalian host. Travel Med Infect Dis. 2010;8:213-22.
59. Hamel R, Dejarnac O, Wichit S, Ekchariyawat P, Neyret A, Luplertlop N, Perera-Lecoin M, Surasombatpattana P, Talignani L, Thomas F, et al. Biology of Zika virus infection in human skin cells. J Virol. 2015;89:8880-96.
60. Aliota MT, Caine EA, Walker EC, Larkin KE, Camacho E, Osorio JE. Characterization of lethal Zika virus infection in AG129 mice. PLoS Negl Trop Dis. 2016;10, e0004682.
61. Taylor RT, Lubick KJ, Robertson SJ, Broughton JP, Bloom ME, Bresnahan WA, Best SM. TRIM79alpha, an interferon-stimulated gene product, restricts tick-borne encephalitis virus replication by degrading the viral RNA polymerase. Cell Host Microbe. 2011;10:185-96.
62. Szretter KJ, Brien JD, Thackray LB, Virgin HW, Cresswell P, Diamond MS. The interferon-inducible gene viperin restricts West Nile virus pathogenesis. J Virol. 2011;85:11557-66.
63. Sheehan KC, Lai KS, Dunn GP, Bruce AT, Diamond MS, Heutel JD, Dungo-Arthur C, Carrero JA, White JM, Hertzog PJ, Schreiber RD. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J Interferon Cytokine Res. 2006;26:804-19.
64. Kurhade C, Zegenhagen L, Weber E, Nair S, Michaelsen-Preusse K, Spanier J, Gekara NO, Kröger A, Överby AK. Type I interferon response in olfactory bulb, the site of tick-borne flavivirus accumulation, is primarily regulated by IPS-1. J Neuroinflammation. 2016;13.
65. Griffin DE. Immune responses to RNA-virus infections of the CNS. Nat Rev Immunol. 2003;3:493-502.
66. Muller U, Steinhoff U, Reis LF, Hemmi S, Pavlovic J, Zinkernagel RM, Aguet M. Functional role of type I and type II interferons in antiviral defense. Science. 1994;264:1918-21.
67. Ryman KD, Klimstra WB, Nguyen KB, Biron CA, Johnston RE. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J Virol. 2000;74:3366-78.
68. Detje CN, Meyer T, Schmidt H, Kreuz D, Rose JK, Bechmann I, Prinz M, Kalinke U. Local type I IFN receptor signaling protects against virus spread within the central nervous system. J Immunol. 2009;182:2297-304.
69. De Miranda J, Yaddanapudi K, Hornig M, Lipkin WI. Astrocytes recognize intracellular polyinosinic-polycytidylic acid via MDA-5. FASEB J. 2009;23:1064-71.
70. Lieberman AP, Pitha PM, Shin HS, Shin ML. Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc Natl Acad Sci U S A. 1989;86:6348-52.
71. Butchi NB, Du M, Peterson KE. Interactions between TLR7 and TLR9 agonists and receptors regulate innate immune responses by astrocytes and microglia. Glia. 2010;58:650-64.
72. Rivieccio MA, Suh HS, Zhao Y, Zhao ML, Chin KC, Lee SC, Brosnan CF. TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for viperin/cig5. J Immunol. 2006;177:4735-41.
73. Pfefferkorn C, Kallfass C, Lienenklaus S, Spanier J, Kalinke U, Rieder M, Conzelmann KK, Michiels T, Staeheli P. Abortively infected astrocytes appear to represent the main source of interferon beta in the virus-infected brain. J Virol. 2015;90:2031-8.
74. Taniguchi T, Takaoka A. A weak signal for strong responses: interferon-alpha/beta revisited. Nat Rev Mol Cell Biol. 2001;2:378-86.
75. Lienenklaus S, Cornitescu M, Zietara N, Lyszkiewicz M, Gekara N, Jablonska J, Edenhofer F, Rajewsky K, Bruder D, Hafner M, et al. Novel reporter mouse reveals constitutive and inflammatory expression of IFN-beta in vivo. J Immunol. 2009;183:3229-36.
76. Kuri T, Zhang X, Habjan M, Martinez-Sobrido L, Garcia-Sastre A, Yuan Z, Weber F. Interferon priming enables cells to partially overturn the SARS coronavirus-induced block in innate immune activation. J Gen Virol. 2009;90:2686-94.
77. Overby AK, Weber F. Hiding from intracellular pattern recognition receptors, a passive strategy of flavivirus immune evasion. Virulence. 2011;2:238-40.
78. Seng LG, Daly J, Chang KC, Kuchipudi SV. High basal expression of interferon-stimulated genes in human bronchial epithelial (BEAS-2B) cells contributes to influenza A virus resistance. PLoS One. 2014;9, e109023.
79. Stirnweiss A, Ksienzyk A, Klages K, Rand U, Grashoff M, Hauser H, Kroger A. IFN regulatory factor-1 bypasses IFN-mediated antiviral effects through viperin gene induction. J Immunol. 2010;184:5179-85.
80. Dai J, Pan W, Wang P. ISG15 facilitates cellular antiviral response to dengue and west Nile virus infection in vitro. Virol J. 2011;8:468.
81. Kajaste-Rudnitski A, Mashimo T, Frenkiel MP, Guenet JL, Lucas M, Despres P. The 2',5'-oligoadenylate synthetase 1b is a potent inhibitor of West Nile virus replication inside infected cells. J Biol Chem. 2006;281:4624-37.
82. Sanda C, Weitzel P, Tsukahara T, Schaley J, Edenberg HJ, Stephens MA, McClintick JN, Blatt LM, Li L, Brodsky L, Taylor MW. Differential gene induction by type I and type II interferons and their combination. J Interferon Cytokine Res. 2006;26:462-72.
83. Metz P, Dazert E, Ruggieri A, Mazur J, Kaderali L, Kaul A, Zeuge U, Windisch MP, Trippler M, Lohmann V, et al. Identification of type I and type II interferon-induced effectors controlling hepatitis C virus replication. Hepatology. 2012;56:2082-93.
84. Crotta S, Davidson S, Mahlakoiv T, Desmet CJ, Buckwalter MR, Albert ML, Staeheli P, Wack A. Type I and type III interferons drive redundant amplification loops to induce a transcriptional signature in influenza-infected airway epithelia. PLoS Pathog. 2013;9, e1003773.
85. Pozner RG, Collado S, Jaquenod de Giusti C, Ure AE, Biedma ME, Romanowski V, Schattner M, Gomez RM. Astrocyte response to Junin virus infection. Neurosci Lett. 2008;445:31-5.
86. Schoneboom BA, Fultz MJ, Miller TH, McKinney LC, Grieder FB. Astrocytes as targets for Venezuelan equine encephalitis virus infection. J Neurovirol. 1999;5:342-54.