The brain parenchyma has a type I interferon response that can limit virus spread

Proceedings of the National Academy of Sciences of the United States of America

Volumn 114, Issue 1, 2017, Pages E95-E104

  Drokhlyansky, Eugene ^a,b   Aytürk, Didem Göz ^a,b   Soh, Timothy K ^a   Chrenek, Ryan ^a,b   O'Loughlin, Elaine ^c   Madore, Charlotte ^c   Butovsky, Oleg ^c   Cepko, Constance L ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Brain|innate immunity; Interferon; Vesicular stomatitis virus; VSV

Indexed keywords

ALPHA INTERFERON RECEPTOR; EBOLA VACCINE; GREEN FLUORESCENT PROTEIN; INTERFERON; INTERLEUKIN 1BETA; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; BRAIN INFECTION; BRAIN TISSUE; CAUDATE NUCLEUS; COMPARATIVE STUDY; CONFERENCE PAPER; CONTROLLED STUDY; DEFECTIVE INTERFERING PARTICLE; GENE EXPRESSION; INNATE IMMUNITY; MALE; MICROGLIA; MOUSE; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PUTAMEN; SIGNAL TRANSDUCTION; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; VESICULOVIRUS; VIRUS CELL INTERACTION; VIRUS PARTICLE; ANIMAL; BRAIN; C57BL MOUSE; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; PARENCHYMA; VESICULAR STOMATITIS; VIROLOGY; VIRUS REPLICATION;

ANIMALS; BRAIN; IMMUNITY, INNATE; INTERFERON TYPE I; MALE; MICE; MICE, INBRED C57BL; PARENCHYMAL TISSUE; VESICULAR STOMATITIS; VESICULOVIRUS; VIRUS REPLICATION;

EID: 85007610480     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1618157114     Document Type: Article

References (78)

1. Galea I, Bechmann I, Perry VH (2007) What is immune privilege (not)? Trends Immunol 28(1):12-18.
2. Murphy JB, Sturm E (1923) Conditions determining the transplantability of tissues in the brain. J Exp Med 38(2):183-197.
3. Stevenson PG, Hawke S, Sloan DJ, Bangham CR (1997) The immunogenicity of intracerebral virus infection depends on anatomical site. J Virol 71(1):145-151.
4. Andersson PB, Perry VH, Gordon S (1992) The acute inflammatory response to lipopolysaccharide in CNS parenchyma differs from that in other body tissues. Neuroscience 48(1):169-186.
5. Bechmann I, Galea I, Perry VH (2007) What is the blood-brain barrier (not)? Trends Immunol 28(1):5-11.
6. Le Bon A, Tough DF (2002) Links between innate and adaptive immunity via type I interferon. Curr Opin Immunol 14(4):432-436.
7. Perry AK, Chen G, Zheng D, Tang H, Cheng G (2005) The host type I interferon response to viral and bacterial infections. Cell Res 15(6):407-422.
8. Delhaye S, et al. (2006) Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci USA 103(20):7835-7840.
9. Kallfass C, et al. (2012) Visualizing production of beta interferon by astrocytes and microglia in brain of La Crosse virus-infected mice. J Virol 86(20):11223-11230.
10. Rock RB, et al. (2004) Role of microglia in central nervous system infections. Clin Microbiol Rev 17(4):942-964.
11. Sorgeloos F, Kreit M, Hermant P, Lardinois C, Michiels T (2013) Antiviral type I and type III interferon responses in the central nervous system. Viruses 5(3):834-857.
12. Rivest S (2009) Regulation of innate immune responses in the brain. Nat Rev Immunol 9(6):429-439.
13. Iannacone M, et al. (2010) Subcapsular sinus macrophages prevent CNS invasion on peripheral infection with a neurotropic virus. Nature 465(7301):1079-1083.
14. Müller U, et al. (1994) Functional role of type I and type II interferons in antiviral defense. Science 264(5167):1918-1921.
15. Beier KT, et al. (2011) Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors. Proc Natl Acad Sci USA 108(37): 15414-15419.
16. Sabin AB, Olitsky PK (1938) Influence of host factors on neuroinvasiveness of vesicular stomatitis virus: III. EFFEct of age and pathway of infection on the character and localization of lesions in the central nervous system. J Exp Med 67(2):201-228.
17. López CB (2014) Defective viral genomes: Critical danger signals of viral infections. J Virol 88(16):8720-8723.
18. Plakhov IV, Aoki C, Reiss CS, Huang AS (1995) Pathogenesis of murine encephalitis limited by defective interfering particles. An immunohistochemical study. J Neurovirol 1(2): 207-218.
19. Doyle M, Holland JJ (1973) Prophylaxis and immunization in mice by use of virus-free defective T particles to protect against intracerebral infection by vesicular stomatitis virus. Proc Natl Acad Sci USA 70(7):2105-2108.
20. Cave DR, Hagen FS, Palma EL, Huang AS (1984) Detection of vesicular stomatitis virus RNA and its defective-interfering particles in individual mouse brains. J Virol 50(1): 86-91.
21. Ransohoff RM, El Khoury J (2015) Microglia in health and disease. Cold Spring Harb Perspect Biol 8(1):a020560, 10.1101/cshperspect.a020560.
22. Nassi JJ, Cepko CL, Born RT, Beier KT (2015) Neuroanatomy goes viral! Front Neuroanat 9(July):80.
23. Beier KT, et al. (2013) Transsynaptic tracing with vesicular stomatitis virus reveals novel retinal circuitry. J Neurosci 33(1):35-51.
24. Marshel JH, Mori T, Nielsen KJ, Callaway EM (2010) Targeting single neuronal networks for gene expression and cell labeling in vivo. Neuron 67(4):562-574.
25. Lichty BD, Power AT, Stojdl DF, Bell JC (2004) Vesicular stomatitis virus: Re-inventing the bullet. Trends Mol Med 10(5):210-216.
26. Geisbert TW, et al. (2008) Vesicular stomatitis virus-based ebola vaccine is well-tolerated and protects immunocompromised nonhuman primates. PLoS Pathog 4(11):e1000225.
27. Parisi SG, et al. (2016) Viral infections of the central nervous system in elderly patients: A retrospective study. Int J Infect Dis 44:8-10.
28. Frensing T (2015) Defective interfering viruses and their impact on vaccines and viral vectors. Biotechnol J 10(5):681-689.
29. Cureton DK, Massol RH, Whelan SPJ, Kirchhausen T (2010) The length of vesicular stomatitis virus particles dictates a need for actin assembly during clathrin-dependent endocytosis. PLoS Pathog 6(9):e1001127.
30. Stauffer Thompson KA, Rempala GA, Yin J (2009) Multiple-hit inhibition of infection by defective interfering particles. J Gen Virol 90(Pt 4):888-899.
31. Drokhlyansky E, Soh TK, Cepko CL (2015) Preferential budding of vesicular stomatitis virus from the basolateral surface of polarized epithelial cells is not solely directed by matrix protein or glycoprotein. J Virol 89(22):11718-11722.
32. Whelan SP, Ball LA, Barr JN, Wertz GT (1995) Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. Proc Natl Acad Sci USA 92(18):8388-8392.
33. Schott DH, Cureton DK, Whelan SP, Hunter CP (2005) An antiviral role for the RNA interference machinery in Caenorhabditis elegans. Proc Natl Acad Sci USA 102(51): 18420-18424.
34. Adler R, Banerjee AK (1976) Analysis of the RNA species isolated from defective particles of vesicular stomatitis virus. J Gen Virol 33(1):51-60.
35. Rehberg E, Kelder B, Hoal EG, Pestka S (1982) Specific molecular activities of recombinant and hybrid leukocyte interferons. J Biol Chem 257(19):11497-11502.
36. Clark K, Plater L, Peggie M, Cohen P (2009) Use of the pharmacological inhibitor BX795 to study the regulation and physiological roles of TBK1 and IkappaB kinase epsilon: A distinct upstream kinase mediates Ser-172 phosphorylation and activation. J Biol Chem 284(21):14136-14146.
37. Quintás-Cardama A, et al. (2010) Preclinical characterization of the selective JAK1/2 inhibitor INCB018424: Therapeutic implications for the treatment of myeloproliferative neoplasms. Blood 115(15):3109-3117.
38. Wu W, Sun X-H (2012) Janus kinase 3: The controller and the controlled. Acta Biochim Biophys Sin (Shanghai) 44(3):187-196.
39. Blank T, Prinz M (2013) Microglia as modulators of cognition and neuropsychiatric disorders. Glia 61(1):62-70.
40. Nayak D, et al. (2013) Type I interferon programs innate myeloid dynamics and gene expression in the virally infected nervous system. PLoS Pathog 9(5):e1003395.
41. Butovsky O, et al. (2014) Identification of a unique TGF-β-dependent molecular and functional signature in microglia. Nat Neurosci 17(1):131-143.
42. Honda K, et al. (2005) IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434(7034):772-777.
43. Lazear HM, et al. (2013) IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog 9(1): e1003118.
44. Grandvaux N, et al. (2002) Transcriptional profiling of interferon regulatory factor 3 target genes: Direct involvement in the regulation of interferon-stimulated genes. J Virol 76(11):5532-5539.
45. Balachandran S, Beg AA (2011) Defining emerging roles for NF-κB in antivirus responses: Revisiting the interferon-β enhanceosome paradigm. PLoS Pathog 7(10): e1002165.
46. Negash AA, et al. (2013) IL-1β production through the NLRP3 inflammasome by hepatic macrophages links hepatitis C virus infection with liver inflammation and disease. PLoS Pathog 9(4):e1003330.
47. Butovsky O, et al. (2012) Modulating inflammatory monocytes with a unique micro-RNA gene signature ameliorates murine ALS. J Clin Invest 122(9):3063-3087.
48. Louveau A, et al. (2015) Structural and functional features of central nervous system lymphatic vessels. Nature 523(7560):337-341.
49. van den Pol AN, Ding S, Robek MD (2014) Long-distance interferon signaling within the brain blocks virus spread. J Virol 88(7):3695-3704.
50. Trottier MD, Lyles DS, Reiss CS (2007) Peripheral, but not central nervous system, type I interferon expression in mice in response to intranasal vesicular stomatitis virus infection. J Neurovirol 13(5):433-445.
51. Detje CN, et al. (2015) Upon intranasal vesicular stomatitis virus infection, astrocytes in the olfactory bulb are important interferon Beta producers that protect from lethal encephalitis. J Virol 89(5):2731-2738.
52. Suzuki J, Osumi N (2015) Neural crest and placode contributions to olfactory development. Curr Top Dev Biol 111:351-374.
53. Faber WM (1937) The nasal mucosa and the subarachnoid space. Am J Anat 62(1): 121-148.
54. Koyuncu OO, Hogue IB, Enquist LW (2013) Virus infections in the nervous system. Cell Host Microbe 13(4):379-393.
55. Lieberman AP, Pitha PM, Shin HS, Shin ML (1989) Production of tumor necrosis factor and other cytokines by astrocytes stimulated with lipopolysaccharide or a neurotropic virus. Proc Natl Acad Sci USA 86(16):6348-6352.
56. Ousman SS, Wang J, Campbell IL (2005) Differential regulation of interferon regulatory factor (IRF)-7 and IRF-9 gene expression in the central nervous system during viral infection. J Virol 79(12):7514-7527.
57. Kreit M, et al. (2014) Inefficient type I interferon-mediated antiviral protection of primary mouse neurons is associated with the lack of apolipoprotein l9 expression. J Virol 88(7):3874-3884.
58. Trottier MD, Jr, Palian BM, Reiss CS (2005) VSV replication in neurons is inhibited by type I IFN at multiple stages of infection. Virology 333(2):215-225.
59. Wollmann G, Robek MD, van den Pol AN (2007) Variable deficiencies in the interferon response enhance susceptibility to vesicular stomatitis virus oncolytic actions in glioblastoma cells but not in normal human glial cells. J Virol 81(3):1479-1491.
60. Fensterl V, et al. (2012) Interferon-induced Ifit2/ISG54 protects mice from lethal VSV neuropathogenesis. PLoS Pathog 8(5):e1002712.
61. Lazear HM, et al. (2015) Interferon-λ restricts West Nile virus neuroinvasion by tightening the blood-brain barrier. Sci Transl Med 7(284):284ra59.
62. Jensen S, Thomsen AR (2012) Sensing of RNA viruses: A review of innate immune receptors involved in recognizing RNA virus invasion. J Virol 86(6):2900-2910.
63. Grabert K, et al. (2016) Microglial brain region-dependent diversity and selective regional sensitivities to aging. Nat Neurosci 19(3):504-516.
64. Sabin AB, Olitsky PK (1937) Influence of host factors on neuroinvasiveness of vesicular stomatitis virus: II. Effect of age on the invasion of the peripheral and central nervous systems by virus injected into the leg muscles or the eye. J Exp Med 66(1):35-57.
65. Macosko EZ, et al. (2015) Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161(5):1202-1214.
66. Habib N, et al. (2016) Div-Seq: Single-nucleus RNA-Seq reveals dynamics of rare adult newborn neurons. Science 353(6302):925-928.
67. Lafon M (2008) Immune evasion, a critical strategy for rabies virus. Dev Biol (Basel) 131:413-419.
68. Piccinotti S, Kirchhausen T, Whelan SPJ (2013) Uptake of rabies virus into epithelial cells by clathrin-mediated endocytosis depends upon actin. J Virol 87(21): 11637-11647.
69. Dargan DJ, Galt CB, Subak-Sharpe JH (1992) The effect of cicloxolone sodium on the replication of vesicular stomatitis virus in BSC-1 cells. J Gen Virol 73(Pt 2):397-406.
70. Cureton DK, Massol RH, Saffarian S, Kirchhausen TL, Whelan SPJ (2009) Vesicular stomatitis virus enters cells through vesicles incompletely coated with clathrin that depend upon actin for internalization. PLoS Pathog 5(4):e1000394.
71. Libert C, Dejager L, Pinheiro I (2010) The X chromosome in immune functions: When a chromosome makes the difference. Nat Rev Immunol 10(8):594-604.
72. Shaw AC, Goldstein DR, Montgomery RR (2013) Age-dependent dysregulation of innate immunity. Nat Rev Immunol 13(12):875-887.
73. Pietzsch T, Preibisch S, Tomancák P, Saalfeld S (2012) ImgLib2-Generic image processing in Java. Bioinformatics 28(22):3009-3011.
74. Schindelin J, et al. (2012) Fiji: An open-source platform for biological-image analysis. Nat Methods 9(7):676-682.
75. Schindelin J, Rueden CT, Hiner MC, Eliceiri KW (2015) The ImageJ ecosystem: An open platform for biomedical image analysis. Mol Reprod Dev 82(7-8):518-529.
76. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-675.
77. Linkert M, et al. (2010) Metadata matters: Access to image data in the real world. J Cell Biol 189(5):777-782.
78. Bissonnette N, Lévesque-Sergerie J-P, Thibault C, Boissonneault G (2009) Spermatozoal transcriptome profiling for bull sperm motility: A potential tool to evaluate semen quality. Reproduction 138(1):65-80.