The Yin and Yang of antiviral innate immunity in central nervous system

Current Pharmaceutical Design

Volumn 22, Issue 6, 2016, Pages 648-655

  Zohaib, Ali ^a   Sarfraz, Adeel ^b   Kaleem, Qari Muhammad ^c   Ye, Jing ^a   Mughal, Mudassar Niaz ^a   Navid, Muhammad Tariq ^a   Khan, Faheem Ahmed ^a   Duan, Xiaodong ^a   Zhu, Bibo ^a   Wan, Shengfeng ^a   Cao, Shengbo ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^b THE ISLAMIA UNIVERSITY OF BAHAWALPUR   (Pakistan)

^c INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Central nervous system; Innate immunity; PAMPs; PRRs; RLRs; TLRs; Virus

Indexed keywords

DNA SENSOR; INTERFERON; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; PROTEIN; RIG I LIKE RECEPTOR; STERILE ALPHA AND TIR MOTIF CONTAINING PROTEIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BRAIN CELL; CELL COMPONENT; CENTRAL NERVOUS SYSTEM; DENDRITIC CELL; GENE; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INNATE IMMUNITY; INTERFERON RESPONSE GENE; MICROGLIA; NON IMMUNE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VIRUS IMMUNITY; CENTRAL NERVOUS SYSTEM INFECTION; CHINESE MEDICINE; IMMUNOLOGY; VIROLOGY;

CENTRAL NERVOUS SYSTEM; CENTRAL NERVOUS SYSTEM VIRAL DISEASES; HUMANS; IMMUNITY, INNATE; RECEPTORS, PATTERN RECOGNITION; YIN-YANG;

EID: 84958267489     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/1381612822666151204001550     Document Type: Article

References (96)

1. Zohaib A, Duan X, Zhu B, et al. The role of ubiquitination in regulation of innate immune signaling. Curr Issues Mol Biol 2015; 30(18): 10.
2. Palm NW, Medzhitov R. Pattern recognition receptors and control of adaptive immunity. Immunol Rev 2009; 227(1): 221-33.
3. Takeuchi O, Akira S. Pattern recognition receptors and inflammation. Cell 2010; 140(6): 805-20.
4. Peltier DC, Simms A, Farmer JR, Miller DJ. Human neuronal cells possess functional cytoplasmic and TLR-mediated innate immune pathways influenced by phosphatidylinositol-3 kinase signaling. J Immunol 2010; 184(12): 7010-21.
5. Nair S, Diamond MS. Innate immune interactions within the central nervous system modulate pathogenesis of viral infections. Curr Opin Immunol 2015; 36: 47-53.
6. de Veer MJ, Holko M, Frevel M, et al. Functional classification of interferon-stimulated genes identified using microarrays. J Leukoc Biol 2001; 69(6): 912-20.
7. Fensterl V, Wetzel JL, Ramachandran S, et al. Interferon-induced Ifit2/ISG54 protects mice from lethal VSV neuropathogenesis. PLoS Pathog 2012; 8(5): e1002712.
8. Takeda K, Kaisho T, Akira S. Toll-like receptors. Annu Rev Immunol 2003; 21: 335-76.
9. O’Neill LAJ, Bowie AG. The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat Rev Immunol 2007; 7(5): 353-64.
10. Paludan SR, Bowie AG, Horan KA, Fitzgerald KA. Recognition of herpesviruses by the innate immune system. Nat Rev Immunol 2011; 11(2): 143-54.
11. Zhang S-Y, Jouanguy E, Ugolini S, et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science 2007; 317(5844): 1522-7.
12. Sancho-Shimizu V, Pérez de Diego R, et al. Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J Clin Invest 2011; 121(12): 4889-902.
13. Pérez de Diego R, Sancho-Shimizu V, Lorenzo L, et al. Human TRAF3 adaptor molecule deficiency leads to impaired Toll-like receptor 3 response and susceptibility to herpes simplex encephalitis. Immunity 2010; 33(3): 400-11.
14. Herman M, Ciancanelli M, Ou YH, et al. Heterozygous TBK1 mutations impair TLR3 immunity and underlie herpes simplex en- cephalitis of childhood. J Exp Med 2012; 209(9): 1567-82.
15. Casrouge A, Zhang S-Y, Eidenschenk C, et al. Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 2006; 314(5797): 308-12.
16. Guo Y, Audry M, Ciancanelli M, et al. Herpes simplex virus encephalitis in a patient with complete TLR3 deficiency: TLR3 is otherwise redundant in protective immunity. J Exp Med 2011; 208(10): 2083-98.
17. Reinert LS, Harder L, Holm CK, 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(4): 1368-76.
18. Menasria R, Boivin N, Lebel M, et al. Both TRIF and IPS-1 adaptor proteins contribute to the cerebral innate immune response against herpes simplex virus 1 infection. J Virol 2013; 87(13): 7301-8.
19. Lafaille FG, Pessach IM, Zhang S-Y, et al. Impaired intrinsic immunity to HSV-1 in human iPSC-derived TLR3-deficient CNS cells. Nature 2012; 491(7426): 769-73.
20. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 2006; 80(10): 5059-64.
21. Orvedahl A, Alexander D, Tallóczy Z, et al. HSV-1 ICP34.5 confers neurovirulence by targeting the Beclin 1 autophagy protein. Cell Host Microbe 2007; 1(1): 23-35.
22. Xu Y, Jagannath C, Liu X-D, et al. Toll-like receptor 4 is a sensor for autophagy associated with innate immunity. Immunity 2007; 27(1): 135-44.
23. Sørensen LN, Reinert LS, Malmgaard L, Bartholdy C, Thomsen AR, Paludan SR. TLR2 and TLR9 Synergistically control herpes simplex virus infection in the brain. J Immunol 2008; 181(12): 8604-12.
24. Lima GK, Zolini GP, Mansur DS, et al. Toll-like receptor (TLR) 2 and TLR9 expressed in trigeminal ganglia are critical to viral control during herpes simplex virus 1 infection. Am J Pathol 2010; 177(5): 2433-45.
25. Krug A, Luker GD, Barchet W, Leib DA, Akira S, Colonna M. Herpes simplex virus type 1 activates murine natural interferon producing cells through toll-like receptor 9. Blood 2004; 103(4): 1433-7.
26. Han YW, Choi JY, Uyangaa E, et al. Distinct dictation of Japanese encephalitis virus-induced neuroinflammation and lethality via triggering TLR3 and TLR4 signal pathways. PLoS Pathog 2014; 10(9): e1004319.
27. Sabouri AH, Marcondes MCG, Flynn C, et al. TLR signaling controls lethal encephalitis in WNV-infected brain. Brain Res 2014; 1574: 84-95.
28. Hidaka F, Matsuo S, Muta T, Takeshige K, Mizukami T, Nunoi H. A missense mutation of the Toll-like receptor 3 gene in a patient with influenza-associated encephalopathy. Clin Immunol 2006; 119(2): 188-94.
29. Hutchens M, Luker KE, Sottile P, et al. TLR3 increases disease morbidity and mortality from vaccinia infection. J Immunol 2008; 180(1): 483-91.
30. Gowen BB, Hoopes JD, Wong MH, et al. TLR3 deletion limits mortality and disease severity due to Phlebovirus infection. J Immunol 2006; 177(9): 6301-7.
31. Le Goffic R, Balloy V, Lagranderie M, et al. Detrimental contribution of the toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog 2006; 2(6): e53.
32. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 2004; 10(12): 1366-73.
33. Daffis S, Samuel MA, Suthar MS, Gale M, Diamond MS. Toll-like receptor 3 has a protective role against West Nile virus infection. J Virol 2008; 82(21): 10349-58.
34. Town T, Bai F, Wang T, et al. Toll-like receptor 7 mitigates lethal West Nile encephalitis via interleukin 23-dependent immune cell infiltration and homing. Immunity 2009; 30(2): 242-53.
35. Aleyas AG, Han YW, Patil AM, Kim SB, Kim K, Eo SK. Impaired cross-presentation of CD8 + CD11c+ dendritic cells by Japanese encephalitis virus in a TLR2/MyD88 signal pathway-dependent manner. Eur J Immunol 2012; 42(10): 2655-66.
36. Faul EJ, Wanjalla CN, Suthar MS, Gale M, Wirblich C, Schnell MJ. Rabies virus infection induces type I interferon production in an IPS-1 dependent manner while dendritic cell activation relies on IFNAR signaling. PLoS Pathog 2010; 6(7): e1001016.
37. Préhaud C, Mégret F, Lafage M, Lafon M. Virus infection switches TLR-3-positive human neurons to become strong producers of beta interferon. J Virol 2005; 79(20): 12893-904.
38. Jackson AC, Rossiter JP, Lafon M. Expression of Toll-like receptor 3 in the human cerebellar cortex in rabies, herpes simplex encephalitis, and other neurological diseases. J Neurovirol 2006; 12(3): 229-34.
39. Ménager P, Roux P, Mégret F, et al. Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS Pathog 2009; 5(2): e1000315.
40. Oshiumi H, Okamoto M, Fujii K, et al. The TLR3/TICAM-1 pathway is mandatory for innate immune responses to poliovirus infection. J Immunol 2011; 187(10): 5320-7.
41. Széles L, Meissner F, Dunand-Sauthier I, et al. TLR3-Mediated CD8+ Dendritic Cell Activation Is Coupled with Establishment of a Cell-Intrinsic Antiviral State. J Immunol 2015; 195(3): 1025-33.
42. Hardarson HS, Baker JS, Yang Z, et al. Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury. Am J Physiol Heart Circ Physiol 2007; 292(1): H251-8.
43. Negishi H, Osawa T, Ogami K, et al. A critical link between Tolllike receptor 3 and type II interferon signaling pathways in antiviral innate immunity. Proc Natl Acad Sci USA 2008; 105(51): 20446-51.
44. Abe Y, Fujii K, Nagata N, et al. The Toll-like receptor 3-mediated antiviral response is important for protection against poliovirus in fection in poliovirus receptor transgenic mice. J Virol 2012; 185-94.
45. Mohanty MC, Deshpande JM. Differential induction of Toll-like receptors & type 1 interferons by Sabin attenuated & wild type 1 polioviruses in human neuronal cells. Indian J Med Res 2013; 138(2): 209-18.
46. Lang KS, Navarini AA, Recher M, et al. MyD88 protects from lethal encephalitis during infection with vesicular stomatitis virus. Eur J Immunol 2007; 37(9): 2434-40.
47. Kim Y, Zhou P, Qian L, et al. MyD88-5 links mitochondria, microtubules, and JNK3 in neurons and regulates neuronal survival. J Exp Med 2007; 204(9): 2063-74.
48. Carty M, Goodbody R, Schröder M, Stack J, Moynagh PN, Bowie AG. The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat Immunol 2006; 7(10): 1074-81.
49. Hou Y-J, Banerjee R, Thomas B, et al. SARM is required for neuronal injury and cytokine production in response to central nervous system viral infection. J Immunol 2013; 191(2): 875-83.
50. Szretter KJ, Samuel MA, Gilfillan S, Fuchs A, Colonna M, Diamond MS. The immune adaptor molecule SARM modulates tumor necrosis factor alpha production and microglia activation in the brainstem and restricts West Nile Virus pathogenesis. J Virol 2009; 83(18): 9329-38.
51. Mukherjee P, Woods TA, Moore RA, Peterson KE. Activation of the innate signaling molecule MAVS by bunyavirus infection upregulates the adaptor protein SARM1, leading to neuronal death. Immunity 2013; 38(4): 705-16.
52. Jiang X, Kinch LN, Brautigam CA, et al. Ubiquitin-induced oligomerization of the RNA sensors RIG-I and MDA5 activates antiviral innate immune response. Immunity 2012; 36(6): 959-73.
53. Michallet M-C, Meylan E, Ermolaeva MA, et al. TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 2008; 28(5): 651-61.
54. Liu S, Chen J, Cai X, et al. MAVS recruits multiple ubiquitin E3 ligases to activate antiviral signaling cascades. eLife 2013; 2; e00785.
55. Rothenfusser S, Goutagny N, DiPerna G, et al. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J Immunol 2005; 175(8): 5260-8. .
56. Satoh T, Kato H, Kumagai Y, et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc Natl Acad Sci USA 2010; 107(4): 1512-7.
57. Chopy D, Pothlichet J, Lafage M, et al. Ambivalent role of the innate immune response in rabies virus pathogenesis. J Virol 2011; 85(13): 6657-68.
58. Lafon M, Mégret F, Meuth SG, et al. Detrimental contribution of the immuno-inhibitor B7-H1 to rabies virus encephalitis. J Immunol 2008; 180(11): 7506-15.
59. Suthar MS, Ma DY, Thomas S, et al. IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog 2010; 6(2): e1000757.
60. Nazmi A, Dutta K, Basu A. RIG-I mediates innate immune response in mouse neurons following Japanese encephalitis virus infection. PloS One 2011; 6(6): e21761.
61. Wollish AC, Ferris MT, Blevins LK, Loo Y-M, Gale M, Heise MT. An attenuating mutation in a neurovirulent Sindbis virus strain interacts with the IPS-1 signaling pathway in vivo. Virology 2013; 435(2): 269-80.
62. Jiang R, Ye J, Zhu B, Song Y, Chen H, Cao S. Roles of TLR3 and RIG-I in mediating the inflammatory response in mouse microglia following Japanese encephalitis virus infection. J Immunol Res 2014; 2014: 787023.
63. Ramos HJ, Lanteri MC, Blahnik G, et al. IL-1 signaling promotes CNS-intrinsic immune control of West Nile virus infection. PLoS Pathog 2012; 8(11): e1003039.
64. Chen C-J, Ou Y-C, Lin S-Y, et al. Glial activation involvement in neuronal death by Japanese encephalitis virus infection. J Gen Virol 2010; 91: 1028-37.
65. Kaushik DK, Gupta M, Kumawat KL, Basu A. NLRP3 inflamma some: key mediator of neuroinflammation in murine Japanese en- cephalitis. PloS One 2012; 7(2): e32270.
66. Nair S, Michaelsen-Preusse K, Finsterbusch K, et al. 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(3):. e1003999.
67. Harikumar KB, Yester JW, Surace MJ, et al. K63-linked polyubiq uitination of transcription factor IRF1 is essential for IL-1-induced production of chemokines CXCL10 and CCL5. Nat Immunol 2014; 15(3): 231-8.
68. Ishikawa H, Ma Z, Barber GN. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 2009; 461(7265): 788-92.
69. Li X-D, Wu J, Gao D, Wang H, Sun L, Chen ZJ. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 2013; 341(6152): 1390-4.
70. Orzalli MH, DeLuca NA, Knipe DM. Nuclear IFI16 induction of IRF-3 signaling during herpesviral infection and degradation of IFI16 by the viral ICP0 protein. Proc Natl Acad Sci USA 2012; 109(44): E3008-17.
71. Ansari MA, Singh VV, Dutta S, et al. Constitutive interferon-inducible protein 16-inflammasome activation during Epstein-Barr virus latency I, II, and III in B and epithelial cells. J Virol 2013; 87(15): 8606-23.
72. Johnson KE, Chikoti L, Chandran B. Herpes simplex virus 1 infection induces activation and subsequent inhibition of the IFI16 and NLRP3 inflammasomes. J Virol 2013; 87(9): 5005-18.
73. Holm CK, Jensen SB, Jakobsen MR, et al. Virus-cell fusion as a trigger of innate immunity dependent on the adaptor STING. Nat Immunol 2012; 13(8): 737-43.
74. Rasmussen SB, Horan KA, Holm CK, et al. Activation of autophagy by alpha-herpesviruses in myeloid cells is mediated by cyto-plasmic viral DNA through a mechanism dependent on STING. J Immunol 2011; 187(10): 5268-76.
75. Luecke S, Paludan SR. Innate recognition of alphaherpesvirus DNA. Adv Virus Res 2015; 92: 63-100.
76. Delhaye S, Paul S, Blakqori G, et al. Neurons produce type I interferon during viral encephalitis. Proc Natl Acad Sci USA 2006; 103(20): 7835-40.
77. Detje CN, Meyer T, Schmidt H, et al. Local type I IFN receptor signaling protects against virus spread within the central nervous system. J Immunol 2009; 182(4): 2297-304.
78. Detje CN, Lienenklaus S, Chhatbar C, et al. Upon intranasal vesicular stomatitis virus infection, astrocytes in the olfactory bulb are important interferon Beta producers that protect from lethal en- cephalitis. J Virol 2015; 89(5): 2731-8.
79. Yordy B, Iijima N, Huttner A, Leib D, Iwasaki A. A neuronspecific role for autophagy in antiviral defense against herpes simplex virus. Cell Host Microbe 2012; 12(3): 334-45.
80. Rosato PC, Leib DA. Intrinsic innate immunity fails to control herpes simplex virus and vesicular stomatitis virus replication in sensory neurons and fibroblasts. J Virol 2014; 88(17): 9991-10001.
81. Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol 2014; 32: 513-45.
82. 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(15): 8363-71.
83. Samuel MA, Whitby K, Keller BC, et al. PKR and RNase L contribute to protection against lethal West Nile Virus infection by con- trolling early viral spread in the periphery and replication in neurons. J Virol 2006; 80(14): 7009-19.
84. 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(22): 11557-66.
85. 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 positivestranded RNA viruses. Nat Med 2013; 19(4): 458-64.
86. Geissmann F, Manz MG, Jung S, Sieweke MH, Merad M, Ley K. Development of monocytes, macrophages, and dendritic cells. Science 2010; 327(5966): 656-61.
87. Serbina NV, Jia T, Hohl TM, Pamer EG. Monocyte-mediated defense against microbial pathogens. Annu Rev Immunol 2008; 26: 421-52.
88. Martinez FO, Helming L, Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 2009; 27: 451-83.
89. Graeber MB. Changing face of microglia. Science 2010; 330(6005): 783-8.
90. Ginhoux F, Greter M, Leboeuf M, et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science 2010; 330(6005): 841-5.
91. Navia BA, Cho ES, Petito CK, Price RW. The AIDS dementia complex: II. Neuropathology. Ann Neurol 1986; 19(6): 525-35.
92. Barnett MH, Parratt JDE, Cho E-S, Prineas JW. Immunoglobulins and complement in postmortem multiple sclerosis tissue. Ann Neurol 2009; 65(1): 32-46.
93. Hickey WF, Kimura H. Perivascular microglial cells of the CNS are bone marrow-derived and present antigen in vivo. Science 1988; 239(4837): 290-2.
94. Mellman I, Steinman RM. Dendritic cells: specialized and regulated antigen processing machines. Cell 2001; 106(3): 255-8.
95. Honda K, Yanai H, Negishi H, et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005; 434(7034): 772-7.
96. van Noort JM, Bsibsi M. Toll-like receptors in the CNS: implications for neurodegeneration and repair. Prog Brain Res 2009; 175: 139-48.