Regional astrocyte IFN signaling restricts pathogenesis during neurotropic viral infection

Journal of Clinical Investigation

Volumn 127, Issue 3, 2017, Pages 843-856

  Daniels, Brian P ^a,b   Jujjavarapu, Harsha ^a   Durrant, Douglas M ^a,c   Williams, Jessica L ^a   Green, Richard R ^b   White, James P ^a   Lazear, Helen M ^a,d   Gale, Michael ^b   Diamond, Michael S ^a   Klein, Robyn S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c CALIFORNIA STATE POLYTECHNIC UNIVERSITY   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2',5' OLIGOADENYLATE SYNTHETASE; ALPHA BETA INTERFERON RECEPTOR; CXCL11 CHEMOKINE; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 1BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; PATTERN RECOGNITION RECEPTOR; RECOMBINANT BETA INTERFERON; TOLL LIKE RECEPTOR 7; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOPATHOLOGY; INNATE IMMUNITY; LEUKOCYTE; MORTALITY; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; VIRAL TROPISM; VIRUS ENCEPHALITIS; VIRUS ENTRY; VIRUS REPLICATION; WEST NILE VIRUS ENCEPHALITIS; WESTERN BLOTTING; ANIMAL; GENETICS; METABOLISM; MUTANT MOUSE STRAIN; PERICYTE; TIGHT JUNCTION; VIROLOGY; WEST NILE FEVER; WEST NILE VIRUS;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; HUMANS; MICE; MICE, MUTANT STRAINS; PERICYTES; RECEPTOR, INTERFERON ALPHA-BETA; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS; WEST NILE FEVER; WEST NILE VIRUS;

EID: 85015888308     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI88720     Document Type: Article

References (68)

1. Platanias LC. Mechanisms of type-I-and type-II-interferon-mediated signalling. Nat Rev Immunol. 2005;5(5):375-386.
2. Lazear HM, Diamond MS. New insights into innate immune restriction of West Nile virus infection. Curr Opin Virol. 2015;11:1-6.
3. Schoggins JW, Rice CM. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol. 2011;1(6):519-525.
4. Daniels BP, Holman DW, Cruz-Orengo L, Jujjavarapu H, Durrant DM, Klein RS. Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals. MBio. 2014;5(5):e01476-e01414.
5. Persidsky Y, Ramirez SH, Haorah J, Kanmogne GD. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol. 2006;1(3):223-236.
6. Daniels BP, Klein RS. Viral sensing at the bloodbrain barrier: new roles for innate immunity at the CNS vasculature. Clin Pharmacol Ther. 2015;97(4):372-379.
7. Pan W, Stone KP, Hsuchou H, Manda VK, Zhang Y, Kastin AJ. Cytokine signaling modulates blood-brain barrier function. Curr Pharm Des. 2011;17(33):3729-3740.
8. Chai Q, He WQ, Zhou M, Lu H, Fu ZF. Enhancement of blood-brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by rabies virus infection. J Virol. 2014;88(9):4698-4710.
9. McCandless EE, Zhang B, Diamond MS, Klein RS. CXCR4 antagonism increases T cell trafficking in the central nervous system and improves survival from West Nile virus encephalitis. Proc Natl Acad Sci USA. 2008;105(32):11270-11275.
10. Zhao L, Toriumi H, Kuang Y, Chen H, Fu ZF. The roles of chemokines in rabies virus infection: overexpression may not always be beneficial. J Virol. 2009;83(22):11808-11818.
11. Wang Y, Lobigs M, Lee E, Müllbacher A. CD8+ T cells mediate recovery and immunopathology in West Nile virus encephalitis. J Virol. 2003;77(24):13323-13334.
12. Furr SR, Marriott I. Viral CNS infections: role of glial pattern recognition receptors in neuroinflammation. Front Microbiol. 2012;3:201.
13. Furr SR, Moerdyk-Schauwecker M, Grdzelishvili VZ, Marriott I. RIG-I mediates nonsegmented negative-sense RNA virus-induced inflammatory immune responses of primary human astrocytes. Glia. 2010;58(13):1620-1629.
14. Pfefferkorn C, et al. Abortively infected astrocytes appear to represent the main source of interferon beta in the virus-infected brain. J Virol. 2015;90(4):2031-2038.
15. Zhang Y, Barres BA. Astrocyte heterogeneity: an underappreciated topic in neurobiology. Curr Opin Neurobiol. 2010;20(5):588-594.
16. Morga E, Faber C, Heuschling P. Regional heterogeneity of the astroglial immunoreactive phenotype: effect of lipopolysaccharide. J Neurosci Res. 1999;57(6):941-952.
17. Fitting S, Zou S, Chen W, Vo P, Hauser KF, Knapp PE. Regional heterogeneity and diversity in cytokine and chemokine production by astroglia: differential responses to HIV-1 Tat, gp120, and morphine revealed by multiplex analysis. J Proteome Res. 2010;9(4):1795-1804.
18. Cho H, Proll SC, Szretter KJ, Katze MG, Gale 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(4):458-464.
19. Hart J, et al. West Nile virus neuroinvasive disease: neurological manifestations and prospective longitudinal outcomes. BMC Infect Dis. 2014;14:248.
20. Shrestha B, Gottlieb D, Diamond MS. Infection and injury of neurons by West Nile encephalitis virus. J Virol. 2003;77(24):13203-13213.
21. Durrant DM, Daniels BP, Klein RS. IL-1R1 signaling regulates CXCL12-mediated T cell localization and fate within the central nervous system during West Nile Virus encephalitis. J Immunol. 2014;193(8):4095-4106.
22. Tao J, et al. Deletion of astroglial Dicer causes non-cell-autonomous neuronal dysfunction and degeneration. J Neurosci. 2011;31(22):8306-8319.
23. Niu W, et al. In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol. 2013;15(10):1164-1175.
24. Howng SY, Huang Y, Ptáek L, Fu YH. Understanding the role of dicer in astrocyte development. PLoS ONE. 2015;10(5):e0126667.
25. Molumby MJ, Keeler AB, Weiner JA. Homophilic protocadherin cell-cell interactions promote dendrite complexity. Cell Rep. 2016;15(5):1037-1050.
26. Pinto AK, et al. Deficient IFN signaling by myeloid cells leads to MAVS-dependent virus-induced sepsis. PLoS Pathog. 2014;10(4):e1004086.
27. Lazear HM, et al. Interferon-restricts West Nile virus neuroinvasion by tightening the blood-brain barrier. Sci Transl Med. 2015;7(284):284ra59.
28. Miner JJ, et al. The TAM receptor Mertk protects against neuroinvasive viral infection by maintaining blood-brain barrier integrity. Nat Med. 2015;21(12):1464-1472.
29. Tedeschi B, Barrett JN, Keane RW. Astrocytes produce interferon that enhances the expression of H-2 antigens on a subpopulation of brain cells. J Cell Biol. 1986;102(6):2244-2253.
30. Keller BC, et al. Resistance to alpha/beta interferon is a determinant of West Nile virus replication fitness and virulence. J Virol. 2006;80(19):9424-9434.
31. Klein RS, et al. Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J Virol. 2005;79(17):11457-11466.
32. Floris S, et al. Interferon-beta directly influences monocyte infiltration into the central nervous system. J Neuroimmunol. 2002;127(1-2):69-79.
33. Bitsch A, et al. Interferon beta-1b modulates serum sVCAM-1 levels in primary progressive multiple sclerosis. Acta Neurol Scand. 2004;110(6):386-392.
34. Calabresi PA, et al. Increases in soluble VCAM-1 correlate with a decrease in MRI lesions in multiple sclerosis treated with interferon beta-1b. Ann Neurol. 1997;41(5):669-674.
35. Engelhardt B, Ransohoff RM. Capture, crawl, cross: the T cell code to breach the blood-brain barriers. Trends Immunol. 2012;33(12):579-589.
36. Gimenez MA, Sim JE, Russell JH. TNFR1-dependent VCAM-1 expression by astrocytes exposes the CNS to destructive inflammation. J Neuroimmunol. 2004;151(1-2):116-125.
37. Archambault AS, Sim J, McCandless EE, Klein RS, Russell JH. Region-specific regulation of inflammation and pathogenesis in experimental autoimmune encephalomyelitis. J Neuroimmunol. 2006;181(1-2):122-132.
38. Getts DR, et al. Targeted blockade in lethal West Nile virus encephalitis indicates a crucial role for very late antigen (VLA)-4-dependent recruitment of nitric oxide-producing macrophages. J Neuroinflammation. 2012;9:246.
39. Stromnes IM, Cerretti LM, Liggitt D, Harris RA, Goverman JM. Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat Med. 2008;14(3):337-342.
40. Rosato PC, Leib DA. Neuronal interferon signaling is required for protection against herpes simplex virus replication and pathogenesis. PLoS Pathog. 2015;11(7):e1005028.
41. Farmer JR, Altschaefl KM, O'Shea KS, Miller DJ. Activation of the type I interferon pathway is enhanced in response to human neuronal differentiation. PLoS ONE. 2013;8(3):e58813.
42. Schultz KL, Vernon PS, Griffin DE. Differentiation of neurons restricts Arbovirus replication and increases expression of the alpha isoform of IRF-7. J Virol. 2015;89(1):48-60.
43. Molofsky AV, et al. Astrocyte-encoded positional cues maintain sensorimotor circuit integrity. Nature. 2014;509(7499):189-194.
44. Sosunov AA, Wu X, Tsankova NM, Guilfoyle E, McKhann GM, Goldman JE. Phenotypic heterogeneity and plasticity of isocortical and hippocampal astrocytes in the human brain. J Neurosci. 2014;34(6):2285-2298.
45. Durrant DM, Robinette ML, Klein RS. IL-1R1 is required for dendritic cell-mediated T cell reactivation within the CNS during West Nile virus encephalitis. J Exp Med. 2013;210(3):503-516.
46. McCandless EE, Budde M, Lees JR, Dorsey D, Lyng E, Klein RS. IL-1R signaling within the central nervous system regulates CXCL12 expression at the blood-brain barrier and disease severity during experimental autoimmune encephalomyelitis. J Immunol. 2009;183(1):613-620.
47. Samuel MA, Wang H, Siddharthan V, Morrey JD, Diamond MS. Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc Natl Acad Sci USA. 2007;104(43):17140-17145.
48. Maximova OA, Bernbaum JG, Pletnev AG. West Nile virus spreads transsynaptically within the pathways of motor control: Anatomical and ultrastructural mapping of neuronal virus infection in the primate central nervous system. PLoS Negl Trop Dis. 2016;10(9):e0004980.
49. Guarda G, et al. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity. 2011;34(2):213-223.
50. Inoue M, Shinohara ML. The role of interferon-in the treatment of multiple sclerosis and experimental autoimmune encephalomyelitis-in the perspective of inflammasomes. Immunology. 2013;139(1):11-18.
51. Moynagh PN. The interleukin-1 signalling pathway in astrocytes: a key contributor to inflammation in the brain. J Anat. 2005;207(3):265-269.
52. An Y, Chen Q, Quan N. Interleukin-1 exerts distinct actions on different cell types of the brain in vitro. J Inflamm Res. 2011;2011(4):11-20.
53. Campbell JH, et al. Anti-4 antibody treatment blocks virus traffic to the brain and gut early, and stabilizes CNS injury late in infection. PLoS Pathog. 2014;10(12):e1004533.
54. Shrestha B, Diamond MS. Role of CD8+ T cells in control of West Nile virus infection. J Virol. 2004;78(15):8312-8321.
55. Szretter KJ, et al. 2'-O methylation of the viral mRNA cap by West Nile virus evades ifit1-dependent and-independent mechanisms of host restriction in vivo. PLoS Pathog. 2012;8(5):e1002698.
56. Ramirez P, et al. BIO5192, a small molecule inhibitor of VLA-4, mobilizes hematopoietic stem and progenitor cells. Blood. 2009;114(7):1340-1343.
57. Ali M, Safriel Y, Sohi J, Llave A, Weathers S. West Nile virus infection: MR imaging findings in the nervous system. AJNR Am J Neuroradiol. 2005;26(2):289-297.
58. Wang HY, Matsui M, Saida T. Immunological disturbances in the central nervous system linked to MRI findings in multiple sclerosis. J Neuroimmunol. 2002;125(1-2):149-154.
59. Khoury SJ, Guttmann CR, Orav EJ, Kikinis R, Jolesz FA, Weiner HL. Changes in activated T cells in the blood correlate with disease activity in multiple sclerosis. Arch Neurol. 2000;57(8):1183-1189.
60. Cramer SP, Modvig S, Simonsen HJ, Frederiksen JL, Larsson HB. Permeability of the blood-brain barrier predicts conversion from optic neuritis to multiple sclerosis. Brain. 2015;138(Pt 9):2571-2583.
61. Rothhammer V, et al. 4-integrins control viral meningoencephalitis through differential recruitment of T helper cell subsets. Acta Neuropathol Commun. 2014;2:27.
62. Le Bon A, et al. Direct stimulation of T cells by type I IFN enhances the CD8+ T cell response during cross-priming. J Immunol. 2006;176(8):4682-4689.
63. Engle MJ, Diamond MS. Antibody prophylaxis and therapy against West Nile virus infection in wild-type and immunodeficient mice. J Virol. 2003;77(24):12941-12949.
64. Ebel GD, et al. Partial genetic characterization of West Nile virus strains, New York State, 2000. Emerging Infect Dis. 2001;7(4):650-653.
65. Beasley DW, Li L, Suderman MT, Barrett AD. Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology. 2002;296(1):17-23.
66. Brien JD, Lazear HM, Diamond MS. Propagation, quantification, detection, and storage of West Nile virus. Curr Protoc Microbiol. 2013;31:15D.3.1-15D.3.18.
67. Lu ZH, et al. The myeloid-binding peptide adenoviral vector enables multi-organ vascular endothelial gene targeting. Lab Invest. 2014;94(8):881-892.
68. Leone DR, et al. An assessment of the mechanistic differences between two integrin alpha 4 beta 1 inhibitors, the monoclonal antibody TA-2 and the small molecule BIO5192, in rat experimental autoimmune encephalomyelitis. J Pharmacol Exp Ther. 2003;305(3):1150-1162.