Genome-wide transcriptional profiling reveals two distinct outcomes in central nervous system infections of rabies virus

Frontiers in Microbiology

Volumn 7, Issue MAY, 2016, Pages

  Zhang, Daiting ^a   He, Feilong ^a   Bi, Shuilian ^b   Guo, Huixia ^a   Zhang, Baoshi ^a   Wu, Fan ^a   Liang, Jiaqi ^a   Yang, Youtian ^a   Tian, Qin ^a   Ju, Chunmei ^a   Fan, Huiying ^a   Chen, Jinding ^a   Guo, Xiaofeng ^a   Luo, Yongwen ^a  

^a SOUTH CHINA AGRICULTURAL UNIVERSITY   (China)

^b GUANGDONG PHARMACEUTICAL UNIVERSITY   (China)

Author keywords

Innate immunity; MHC class II; Pathogenesis; Pathogenic and attenuated strains; Rabies virus; Transcriptome

Indexed keywords

GAMMA INTERFERON; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CENTRAL NERVOUS SYSTEM INFECTION; CONTROLLED STUDY; ENCEPHALITIS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; GENE ONTOLOGY; GENETIC ASSOCIATION; HIGH THROUGHPUT SEQUENCING; HISTOLOGY; IMMUNOREGULATION; MOUSE; NEUROBLASTOMA; NEUROPATHOLOGY; NEUROTRANSMISSION; NEWCASTLE DISEASE VIRUS; NONHUMAN; RABIES VIRUS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SYNAPTIC TRANSMISSION; VIRAL CLEARANCE; WESTERN BLOTTING;

EID: 84973571881     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00751     Document Type: Article

References (64)

1. Akaike, T., Weihe, E., Schaefer, M., Fu, Z. F., Zheng, Y. M., Vogel, W., et al. (1995). Effect of neurotropic virus infection on neuronal and inducible nitric oxide synthase activity in rat brain. J. Neurovirol. 1, 118-125. doi: 10.3109/13550289509111016
2. Anders, S., and Huber, W. (2010). Differential expression analysis for sequence count data. Genome Biol. 11:R106. doi: 10.1186/gb-2010-11-10-r106
3. Arroyo, A. G., and Iruela-Arispe, M. L. (2010). Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc. Res. 86, 226-235. doi: 10.1093/cvr/cvq049
4. Bai, S. W., Herrera-Abreu, M. T., Rohn, J. L., Racine, V., Tajadura, V., Suryavanshi, N., et al. (2011). Identification and characterization of a set of conserved and new regulators of cytoskeletal organization, cell morphology and migration. BMC Biol. 9:54. doi: 10.1186/1741-7007-9-54
5. Blondel, D., Kheddache, S., Lahaye, X., Dianoux, L., and Chelbi-Alix, M. K. (2010). Resistance to rabies virus infection conferred by the PMLIV isoform. J. Virol. 84, 10719-10726. doi: 10.1128/JVI.01286-10
6. Brzozka, K., Finke, S., and Conzelmann, K. K. (2005). Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 79, 7673-7681. doi: 10.1128/JVI.79.12.7673-7681.2005
7. Brzozka, K., Finke, S., and Conzelmann, K. K. (2006). Inhibition of interferon signaling by rabies virus phosphoprotein P: activation-dependent binding of STAT1 and STAT2. J. Virol. 80, 2675-2683. doi: 10.1128/JVI.80.6.2675-2683.2006
8. Carman, A. J., Mills, J. H., Krenz, A., Kim, D. G., and Bynoe, M. S. (2011). Adenosine receptor signaling modulates permeability of the blood-brain barrier. J. Neurosci. 31, 13272-13280. doi: 10.1523/JNEUROSCI.3337-11.2011
9. Carmeliet, P. (2000). Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6, 389-395. doi: 10.1038/74651
10. Chai, Q., He, W. Q., Zhou, M., Lu, H., and Fu, Z. F. (2014). 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. 88, 4698-4710. doi: 10.1128/JVI.03149-13
11. Chelbi-Alix, M. K., Vidy, A., El Bougrini, J., and Blondel, D. (2006). Rabies viral mechanisms to escape the IFN system: the viral protein P interferes with IRF-3, Stat1, and PML nuclear bodies. J. Interferon Cytokine Res. 26, 271-280. doi: 10.1089/jir.2006.26.271
12. Chopy, D., Detje, C. N., Lafage, M., Kalinke, U., and Lafon, M. (2011a). The type I interferon response bridles rabies virus infection and reduces pathogenicity. J. Neurovirol. 17, 353-367. doi: 10.1007/s13365-011-0041-6
13. Chopy, D., Pothlichet, J., Lafage, M., Megret, F., Fiette, L., Si-Tahar, M., et al. (2011b). Ambivalent role of the innate immune response in rabies virus pathogenesis. J. Virol. 85, 6657-6668. doi: 10.1128/JVI.00302-11
14. Dhingra, V., Li, X., Liu, Y., and Fu, Z. F. (2007). Proteomic profiling reveals that rabies virus infection results in differential expression of host proteins involved in ion homeostasis and synaptic physiology in the central nervous system. J. Neurovirol. 13, 107-117. doi: 10.1080/13550280601178226
15. Faber, M., Li, J., Kean, R. B., Hooper, D. C., Alugupalli, K. R., and Dietzschold, B. (2009). Effective preexposure and postexposure prophylaxis of rabies with a highly attenuated recombinant rabies virus. Proc. Natl. Acad. Sci. U.S.A. 106, 11300-11305. doi: 10.1073/pnas.0905640106
16. Faul, E. J., Wanjalla, C. N., Suthar, M. S., Gale, M., Wirblich, C., and Schnell, M. J. (2010). Rabies virus infection induces type I interferon production in an IPS-1 dependent manner while dendritic cell activation relies on IFNAR signaling. PLoS Pathog. 6:e1001016. doi: 10.1371/journal.ppat.1001016
17. Fooks, A. R., Banyard, A. C., Horton, D. L., Johnson, N., McElhinney, L. M., and Jackson, A. C. (2014). Current status of rabies and prospects for elimination. Lancet 384, 1389-1399. doi: 10.1016/S0140-6736(13)62707-5
18. Fu, Z. F., and Jackson, A. C. (2005). Neuronal dysfunction and death in rabies virus infection. J. Neurovirol. 11, 101-106. doi: 10.1080/13550280590900445
19. Galelli, A., Baloul, L., and Lafon, M. (2000). Abortive rabies virus central nervous infection is controlled by T lymphocyte local recruitment and induction of apoptosis. J. Neurovirol. 6, 359-372. doi: 10.3109/13550280009018300
20. Gnanadurai, C. W., Yang, Y., Huang, Y., Li, Z., Leyson, C. M., Cooper, T. L., et al. (2015). Differential host immune responses after infection with wild-type or lab-attenuated rabies viruses in dogs. PLoS Negl. Trop. Dis. 9:e0004023. doi: 10.1371/journal.pntd.0004023
21. Hooper, D. C., Phares, T. W., Fabis, M. J., and Roy, A. (2009). The production of antibody by invading B cells is required for the clearance of rabies virus from the central nervous system. PLoS Negl. Trop. Dis. 3:e535. doi: 10.1371/journal.pntd.0000535
22. Hooper, D. C., Roy, A., Barkhouse, D. A., Li, J., and Kean, R. B. (2011). Rabies virus clearance from the central nervous system. Adv. Virus Res. 79, 55-71. doi: 10.1016/B978-0-12-387040-7.00004-4
23. Hornung, V., Ellegast, J., Kim, S., Brzozka, K., Jung, A., Kato, H., et al. (2006). 5'-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997. doi: 10.1126/science.1132505
24. Huang da, W., Sherman, B. T., and Lempicki, R. A. (2009). Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57. doi: 10.1038/nprot.2008.211
25. Iwata, M., Komori, S., Unno, T., Minamoto, N., and Ohashi, H. (1999). Modification of membrane currents in mouse neuroblastoma cells following infection with rabies virus. Br. J. Pharmacol. 126, 1691-1698. doi: 10.1038/sj.bjp.0702473
26. Iwata, M., Unno, T., Minamoto, N., Ohashi, H., and Komori, S. (2000). Rabies virus infection prevents the modulation by alpha(2)-adrenoceptors, but not muscarinic receptors, of Ca(2+) channels in NG108-15 cells. Eur. J. Pharmacol. 404, 79-88. doi: 10.1016/S0014-2999(00)00621-X
27. Jensen, S., and Thomsen, A. R. (2012). Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. J. Virol. 86, 2900-2910. doi: 10.1128/JVI.05738-11
28. Johnson, N., McKimmie, C. S., Mansfield, K. L., Wakeley, P. R., Brookes, S. M., Fazakerley, J. K., et al. (2006). Lyssavirus infection activates interferon gene expression in the brain. J. Gen. Virol. 87, 2663-2667. doi: 10.1099/vir.0.82024-0
29. Klein, R. S., Lin, E., Zhang, B., Luster, A. D., Tollett, J., Samuel, M. A., et al. (2005). Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J. Virol. 79, 11457-11466. doi: 10.1128/JVI.79.17.11457-11466.2005
30. Lafon, M. (2005). Modulation of the immune response in the nervous system by rabies virus. Curr. Top. Microbiol. Immunol. 289, 239-258. doi: 10.1007/3-540-27320-4_11
31. Lafon, M. (2011). Evasive strategies in rabies virus infection. Adv. Virus Res. 79, 33-53. doi: 10.1016/B978-0-12-387040-7.00003-2
32. Li, D., Qian, L., Chen, C., Shi, M., Yu, M., Hu, M., et al. (2009). Down-regulation of MHC class II expression through inhibition of CIITA transcription by lytic transactivator Zta during Epstein-Barr virus reactivation. J. Immunol. 182, 1799-1809. doi: 10.4049/jimmunol.0802686
33. Li, J., Ertel, A., Portocarrero, C., Barkhouse, D. A., Dietzschold, B., Hooper, D. C., et al. (2012). Postexposure treatment with the live-attenuated rabies virus (RV) vaccine TriGAS triggers the clearance of wild-type RV from the Central Nervous System (CNS) through the rapid induction of genes relevant to adaptive immunity in CNS tissues. J. Virol. 86, 3200-3210. doi: 10.1128/JVI.06699-11
34. Li, J., Faber, M., Dietzschold, B., and Hooper, D. C. (2011). The role of toll-like receptors in the induction of immune responses during rabies virus infection. Adv. Virus Res. 79, 115-126. doi: 10.1016/B978-0-12-387040-7.00007-X
35. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408. doi: 10.1006/meth.2001.1262
36. Marcovistz, R., Germano, P. M., Riviere, Y., Tsiang, H., and Hovanessian, A. G. (1987). The effect of interferon treatment in rabies prophylaxis in immunocompetent, immunosuppressed, and immunodeficient mice. J. Interferon Res. 7, 17-27. doi: 10.1089/jir.1987.7.17
37. Marques, C. P., Kapil, P., Hinton, D. R., Hindinger, C., Nutt, S. L., Ransohoff, R. M., et al. (2011). CXCR3-dependent plasma blast migration to the central nervous system during viral encephalomyelitis. J. Virol. 85, 6136-6147. doi: 10.1128/JVI.00202-11
38. Masatani, T., Ito, N., Shimizu, K., Ito, Y., Nakagawa, K., Sawaki, Y., et al. (2010). Rabies virus nucleoprotein functions to evade activation of the RIG-I-mediated antiviral response. J. Virol. 84, 4002-4012. doi: 10.1128/JVI.02220-09
39. Matza, D., Kerem, A., and Shachar, I. (2003). Invariant chain, a chain of command. Trends Immunol. 24, 264-268. doi: 10.1016/S1471-4906(03)00073-5
40. Melchjorsen, J., Sorensen, L. N., and Paludan, S. R. (2003). Expression and function of chemokines during viral infections: from molecular mechanisms to in vivo function. J. Leukoc. Biol. 74, 331-343. doi: 10.1189/jlb.1102577
41. Mitrabhakdi, E., Shuangshoti, S., Wannakrairot, P., Lewis, R. A., Susuki, K., Laothamatas, J., et al. (2005). Difference in neuropathogenetic mechanisms in human furious and paralytic rabies. J. Neurol. Sci. 238, 3-10. doi: 10.1016/j.jns.2005.05.004
42. Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628. doi: 10.1038/nmeth.1226
43. Moutaftsi, M., Mehl, A. M., Borysiewicz, L. K., and Tabi, Z. (2002). Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells. Blood 99, 2913-2921. doi: 10.1182/blood. V99.8.2913
44. Muller, M., Carter, S., Hofer, M. J., and Campbell, I. L. (2010). Review: the chemokine receptor CXCR3 and its ligands CXCL9, CXCL10 and CXCL11 in neuroimmunity-a tale of conflict and conundrum. Neuropathol. Appl. Neurobiol. 36, 368-387. doi: 10.1111/j.1365-2990.2010.01089.x
45. Niu, X., Wang, H., and Fu, Z. F. (2011). Role of chemokines in rabies pathogenesis and protection. Adv. Virus Res. 79, 73-89. doi: 10.1016/B978-0-12-387040-7.00005-6
46. Oh, S. W., Onomoto, K., Wakimoto, M., Onoguchi, K., Ishidate, F., Fujiwara, T., et al. (2016). Leader-containing uncapped viral transcript activates RIG-I in antiviral stress granules. PLoS Pathog. 12:e1005444. doi: 10.1371/journal.ppat.1005444
47. Phares, T. W., Kean, R. B., Mikheeva, T., and Hooper, D. C. (2006). Regional differences in blood-brain barrier permeability changes and inflammation in the apathogenic clearance of virus from the central nervous system. J. Immunol. 176, 7666-7675. doi: 10.4049/jimmunol.176.12.7666
48. Postic, B., and Fenje, P. (1971). Effect of administered interferon on rabies in rabbits. Appl. Microbiol. 22, 428-431
49. Rieder, M., and Conzelmann, K. K. (2009). Rhabdovirus evasion of the interferon system. J. Interferon Cytokine Res. 29, 499-509. doi: 10.1089/jir.2009.0068
50. Roy, A., Phares, T. W., Koprowski, H., and Hooper, D. C. (2007). Failure to open the blood-brain barrier and deliver immune effectors to central nervous system tissues leads to the lethal outcome of silver-haired bat rabies virus infection. J. Virol. 81, 1110-1118. doi: 10.1128/JVI.01964-06
51. Schnell, M. J., McGettigan, J. P., Wirblich, C., and Papaneri, A. (2010). The cell biology of rabies virus: using stealth to reach the brain. Nat. Rev. Microbiol. 8, 51-61. doi: 10.1038/nrmicro2260
52. Spiegel, I., Mardinly, A. R., Gabel, H. W., Bazinet, J. E., Couch, C. H., Tzeng, C. P., et al. (2014). Npas4 regulates excitatory-inhibitory balance within neural circuits through cell-type-specific gene programs. Cell 157, 1216-1229. doi: 10.1016/j.cell.2014.03.058
53. Sugiura, N., Uda, A., Inoue, S., Kojima, D., Hamamoto, N., Kaku, Y., et al. (2011). Gene expression analysis of host innate immune responses in the central nervous system following lethal CVS-11 infection in mice. Jpn. J. Infect. Dis. 64, 463-472
54. Sun, Y., Ding, N., Ding, S. S., Yu, S., Meng, C., Chen, H., et al. (2013). Goose RIG-I functions in innate immunity against Newcastle disease virus infections. Mol. Immunol. 53, 321-327. doi: 10.1016/j.molimm.2012.08.022
55. Takayama-Ito, M., Inoue, K., Shoji, Y., Inoue, S., Iijima, T., Sakai, T., et al. (2006). A highly attenuated rabies virus HEP-Flury strain reverts to virulent by single amino acid substitution to arginine at position 333 in glycoprotein. Virus Res. 119, 208-215. doi: 10.1016/j.virusres.2006.01.014
56. Ting, J. P., and Trowsdale, J. (2002). Genetic control of MHC class II expression. Cell 109 (suppl.), S21-S33. doi: 10.1016/s0092-8674(02)00696-7
57. Vidy, A., Chelbi-Alix, M., and Blondel, D. (2005). Rabies virus P protein interacts with STAT1 and inhibits interferon signal transduction pathways. J. Virol. 79, 14411-14420. doi: 10.1128/JVI.79.22.14411-14420.2005
58. Wang, Z. W., Sarmento, L., Wang, Y., Li, X. Q., Dhingra, V., Tseggai, T., et al. (2005). Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J. Virol. 79, 12554-12565. doi: 10.1128/JVI.79.19.12554-12565.2005
59. Yang, J. Y., Dunker, A., Liu, J. S., Qin, X., Arabnia, H. R., Yang, W., et al. (2014). Advances in translational bioinformatics facilitate revealing the landscape of complex disease mechanisms. BMC Bioinformatics 15 (suppl. 17):I1. doi: 10.1186/1471-2105-15-S17-I1
60. Yang, Y., Huang, Y., Gnanadurai, C. W., Cao, S., Liu, X., Cui, M., et al. (2015). The inability of wild-type rabies virus to activate dendritic cells is dependent on the glycoprotein and correlates with its low level of the de novo-synthesized leader RNA. J. Virol. 89, 2157-2169. doi: 10.1128/JVI.02092-14
61. Zandi, F., Eslami, N., Soheili, M., Fayaz, A., Gholami, A., and Vaziri, B. (2009). Proteomics analysis of BHK-21 cells infected with a fixed strain of rabies virus. Proteomics 9, 2399-2407. doi: 10.1002/pmic.200701007
62. Zhao, L., Toriumi, H., Kuang, Y., Chen, H., and Fu, Z. F. (2009). The roles of chemokines in rabies virus infection: overexpression may not always be beneficial. J. Virol. 83, 11808-11818. doi: 10.1128/JVI.01346-09
63. Zhao, L., Toriumi, H., Wang, H., Kuang, Y., Guo, X., Morimoto, K., et al. (2010). Expression of MIP-1alpha (CCL3) by a recombinant rabies virus enhances its immunogenicity by inducing innate immunity and recruiting dendritic cells and B cells. J. Virol. 84, 9642-9648. doi: 10.1128/JVI.00326-10
64. Zhao, P., Zhao, L., Zhang, T., Qi, Y., Wang, T., Liu, K., et al. (2011). Innate immune response gene expression profiles in central nervous system of mice infected with rabies virus. Comp. Immunol. Microbiol. Infect. Dis. 34, 503-512. doi: 10.1016/j.cimid.2011.09.003